AN INVESTIGATION OF THE ACE INHIBITORY ACTIVITY, ANTIOXIDANT CAPACITY, AND PHYTOCHEMICAL CONSTITUENTS OF POLAR AND NON-POLAR EXTRACTS OF ZIZIPHUS JUJUBA FRUIT: STATISTICAL SCREENING THE MAIN COMPONENTS RESPONSIBLE FOR BIOACTIVITY

Öz

Herein, the angiotensin I-converting enzyme (ACE) inhibitory activity, antioxidant capacity, total polyphenol contents (TPC), and phytochemical profiles of polar and non-polar extracts of dried Ziziphus jujuba fruits were investigated, along with the statistical determination of the main components responsible for ACE inhibitory activity. The non-polar extract expressed the strongest ACE inhibitory activity (99.81%) among the extracts. The non-polar extract also exhibited the highest DPPH scavenging activity (IC50 of 30.63), linoleic acid/β-carotene bleaching capacity (89.31%), and TPC (59.47 mg GAE/g). The phenolic profiles of the extracts were identified by LC-MS/MS, and the presence of seven triterpenoid species in the extracts was examined using GC-MS techniques. The principal constituents included 19 phenolics, 2 organic acids, and 4 triterpenoids. A Pearson correlation and principal component analysis were conducted to find the correlation between individual phenolic compounds and ACE inhibitory activity.

Anahtar Kelimeler

• Ziziphus jujuba
• ACE inhibitory activity
• antioxidant capacity
• phytochemical profile
• Pearson correlation
• principal component analysis

ZIZIPHUS JUJUBA (HÜNNAP) MEYVESİNİN POLAR VE APOLAR EKSTRAKLARININ ACE İNHİBİTÖR AKTİVİTESİ, ANTİOKSİDAN KAPASİTESİ VE FİTOKİMYASAL BİLEŞENLERİNİN İNCELENMESİ: BİYOAKTİVİTEDEN SORUMLU ANA BİLEŞENLERİN İSTATİSTİKSEL İNCELENMESİ

Öz

Bu çalışmada Ziziphus jujuba’nın kurutulmuş meyvelerinin polar ve apolar ekstraktlarının anjiyotensin I-dönüştürücü enzim (ACE) inhibitör aktivitesi, antioksidan kapasitesi, toplam polifenol içerikleri (TPC) ve fitokimyasal profilleri araştırılmıştır ve ACE inhibitör aktivitesinden sorumlu temel bileşenler istatistiksel olarak analiz edilmiştir. En yüksek ACE inhibitör aktivitesi (%99.81) meyvenin apolar ekstraktında tespit edilmiştir. Apolar ekstrakt ayrıca en yüksek DPPH radikal süpürme aktivitesi (IC50 : 30,63), linoleik asit/β-karoten ağartma kapasitesi (%89.31) ve TPC'yi (59.47 mg GAE/g) sergilemiştir. Ekstraktların fenolik profilleri LC-MS/MS ile tanımlanmış ve ekstraktlardaki yedi triterpenoid türünün varlığı GC-MS teknikleri kullanılarak incelenmiş ve 19 fenolik, 2 organik asit ve 4 triterpenoid tanımlanmıştır. ACE inhibisyon aktivitesinden sorumlu fenolik bileşenlerin belirlenmesi amacı ile Pearson korelasyonu ve temel bileşen analizi kullanılmıştır.

Anahtar Kelimeler

• Ziziphus jujuba
• ACE inhibitory activity
• antioxidant capacity
• phytochemical profile
• Pearson correlation
• principal component analysis

Kaynakça

1. Agunloye, O. M., Oboh, G. (2018). Caffeic acid and chlorogenic acid: Evaluation of antioxidant effect and inhibition of key enzymes linked with hypertension. Journal of Food Biochemistry, 42(4): e12541. https://doi.org/10.1111/jfbc.12541
2. Ali, M. Y., Seong, S. H., Jung, H. A., Choi, J. S. (2019). Angiotensin-I-converting enzyme inhibitory activity of coumarins from Angelica decursiva. Molecules, 24(21). https://doi.org/ 10.3390/molecules24213937
3. Al-Saeedi, A. H., Al- Ghafri, M. T. H., Hossain, M. A. (2016). Comparative evaluation of total phenols, flavonoids content and antioxidant potential of leaf and fruit extracts of Omani Ziziphus jujuba L. Pacific Science Review A: Natural Science and Engineering, 18(1): 78–83. https://doi.org/10.1016/J.PSRA.2016.09.001
4. Bakir, D., Akdeniz, M., Ertas, A., Yilmaz, M. A., Yener, I., Firat, M., Kolak, U. (2020). A GC–MS method validation for quantitative investigation of some chemical markers in Salvia hypargeia Fisch. & C.A. Mey. of Turkey: Enzyme inhibitory potential of ferruginol. Journal of Food Biochemistry, 44(9): e13350. https://doi.org/10.1111/ jfbc.13350
5. Castellano, J. M., Ramos-Romero, S., Perona, J. S. (2022). Oleanolic Acid: Extraction, characterization and biological activity. Nutrients, 14(3): 623.
6. Ciniviz, M., Yildiz, H. (2020). Determination of phenolic acid profiles by HPLC in lacto-fermented fruits and vegetables (pickle): Effect of pulp and juice portions. Journal of Food Processing and Preservation, 44(7): 1–11. https://doi.org/10.1111/jfpp.14542
7. Gil-Martín, E., Forbes-Hernández, T., Romero, A., Cianciosi, D., Giampieri, F., Battino, M. (2022). Influence of the extraction method on the recovery of bioactive phenolic compounds from food industry by-products. Food Chemistry, 378: 131918. https://doi.org/10.1016/ J.FOODCHEM.2021.131918
8. Guerrero, L., Castillo, J., Quiñones, M., Garcia-Vallvé, S., Arola, L., Pujadas, G., Muguerza, B. (2012). Inhibition of Angiotensin-converting enzyme activity by flavonoids: Structure-activity relationship studies. PLOS ONE, 7(11): e49493.

9. Hernández, F., Noguera-Artiaga, L., Burló, F., Wojdyło, A., Carbonell-Barrachina, Á. A., Legua, P. (2016). Physico-chemical, nutritional, and volatile composition and sensory profile of Spanish jujube (Ziziphus jujuba Mill.) fruits. Journal of the Science of Food and Agriculture, 96(8): 2682–2691. https://doi.org/10.1002/jsfa.7386
10. Hui, Z., Wen, H., Zhu, J., Deng, H., Jiang, X., Ye, X. Y., Wang, L., Xie, T., Bai, R. (2024). Discovery of plant-derived anti-tumor natural products: Potential leads for anti-tumor drug discovery. Bioorganic Chemistry, 142: 106957. https://doi.org/10.1016/J.BIOORG.2023.106957
11. Kamkar-Del, Y., Mohebbati, R., Hosseini, M., Khajavir, A., Shafei, M., Rakhshandeh, H. (2020). Ethyl acetate and aqueous fractions of Ziziphus jujuba prevent acute hypertension induced by Angiotensin II in rats. Cardiovasc Hematol Disord Drug Targets, 20(2): 108-115. https://doi.org/ 10.2174/1871529X19666191119141400
12. Kwon, Y. I., Vattem, D. A., Shetty, K. (2006). Evaluation of clonal herbs of Lamiaceae species for management of diabetes and hypertension. Asia Pacific Journal of Clinical Nutrition, 15:107–118.
13. Li, D., Yue, D., Liu, D., Zhang, L., Song, S. (2020). Phytochemical and chemotaxonomic study on Ziziphus jujuba Mill. (Rhamnaceae). Biochemical Systematics and Ecology, 91: 104058. https://doi.org/10.1016/J.BSE.2020.104058
14. Lin, Y. S., Lin, W. S., Tung, J. W., Cheng, Y. C., Chang, M. Y., Chen, C. Y., Huang, S. L. (2020). Antioxidant capacities of jujube fruit seeds and peel pulp. Applied Sciences (Switzerland), 10(17):6007. https://doi.org/10.3390/ app10176007
15. Memarpoor-Yazdi, M., Zare-Zardini, H., Mogharrab, N., Navapour, L. (2020). Purification, characterization and mechanistic evaluation of angiotensin converting enzyme inhibitory peptides derived from Zizyphus jujuba fruit. Scientific Reports, 10(1): 3976. https://doi.org/10.1038/s41598-020-60972-w
16. Meng, J., Fang, Y., Zhang, A., Chen, S., Xu, T., Ren, Z., Han, G., Liu, J., Li, H., Zhang, Z., Wang, H. (2011). Phenolic content and antioxidant capacity of Chinese raisins produced in Xinjiang Province. Food Research International, 44(9): 2830–2836. https://doi.org/10.1016/ j.foodres.2011.06.032
17. Ng, Z. X., Soh, E. Y. W., Yong, P. H. (2022). The influence of fermentation and drying methods on the functional activities and sensory quality of Artemisia argyi H.Lév. & Vaniot herbal tea. Journal of Applied Research on Medicinal and Aromatic Plants, 30: 100393. https://doi.org/10.1016/ J.JARMAP.2022.100393
18. Oliveira, A. C. de, Mar, J. M., Corrêa, R. F., Sanches, E. A., Campelo, P. H., Ramos, A. da S., Bezerra, J. de A. (2023). Pouteria spp. fruits: Health benefits of bioactive compounds and their potential for the food industry. Food Research International, 173: 113310. https://doi.org/ 10.1016/J.FOODRES.2023.113310
19. Paiva, L., Lima, E., Marcone, M., Baptista, J. (2023). Angiotensin I-converting enzyme (ACE) inhibition and biological activities of green and black tea samples from Azorean Camellia sinensis. Journal of Functional Foods, 107: 105701. https://doi.org/10.1016/J.JFF.2023.105701
20. Pan, F., Zhao, X., Liu, F., Luo, Z., Chen, S., Liu, Z., Zhao, Z., Liu, M., Wang, L. (2023). Triterpenoids in jujube: A review of composition, content diversity, pharmacological effects, synthetic pathway, and variation during domestication. Plants, 12(7): 1501 https://doi.org/10.3390/plants12071501
21. Ruiz Rodríguez, L. G., Zamora Gasga, V. M., Pescuma, M., Van Nieuwenhove, C., Mozzi, F., Sánchez Burgos, J. A. (2021). Fruits and fruit by-products as sources of bioactive compounds. Benefits and trends of lactic acid fermentation in the development of novel fruit-based functional beverages. Food Research International, 140: 109854. https://doi.org/10.1016/J.FOODRES.2020.109854
22. Safaeian, L., Emami, R., Hajhashemi, V., Haghighatian, Z. (2018). Antihypertensive and antioxidant effects of protocatechuic acid in deoxycorticosterone acetate-salt hypertensive rats. Biomedicine & Pharmacotherapy, 100: 147–155. https://doi.org/10.1016/J.BIOPHA.2018.01.107
23. Saleem, H., Yaqub, A., Rafique, R., Ali Chohan, T., Malik, D.-S., Tousif, M. I., Khurshid, U., Ahemad, N., Ramasubburayan, R., Rengasamy, K. R. R. (2023). Nutritional and medicinal plants as potential sources of enzyme inhibitors toward the bioactive functional foods: An updated review. Critical Reviews in Food Science and Nutrition, 1–24. https://doi.org/10.1080/ 10408398.2023.2217264
24. Şensu, E., Duran, A., Özcelik, B., Yucetepe, A. (2023). Investigation of changes in some bioactive properties of phenolic extracts from pulp and seed tissues of Ziziphus jujuba during in vitro digestion. Gıda, 48(3): 602–613. https://doi.org/10.15237/gida.gd23033
25. Song, L., Zhang, L., Xu, L., Ma, Y., Lian, W., Liu, Y., Wang, Y. (2020). Optimized Extraction of Total Triterpenoids from Jujube (Ziziphus jujuba Mill.) and Comprehensive Analysis of Triterpenic Acids in Different Cultivars. Plants, 9(4): 412 https://doi.org/10.3390/plants9040412
26. Wang, B., Huang, Q., Venkitasamy, C., Chai, H., Gao, H., Cheng, N., Cao, W., Lv, X., Pan, Z. (2016). Changes in phenolic compounds and their antioxidant capacities in jujube (Ziziphus jujuba Miller) during three edible maturity stages. LWT - Food Science and Technology, 66: 56–62. https://doi.org/10.1016/J.LWT.2015.10.005
27. Wink, M. (2010). Functions and biotechnology of plant secondary metabolites. Annual Plant Reviews, (39). Wiley-Blackwell Publishing Ltda, USA.
28. Wu, N., Zhao, Y., Wang, Y., Shuang, Q. (2022). Effects of ultra-high pressure treatment on angiotensin-converting enzyme (ACE) inhibitory activity, antioxidant activity, and physicochemical properties of milk fermented with Lactobacillus delbrueckii QS306. Journal of Dairy Science, 105(3): 1837–1847. https://doi.org/10.3168/JDS.2021-20990
29. Yamamoto, M., Suzuki, A., Hase, T. (2008). Short-term effects of glucosyl hesperidin and hesperetin on blood pressure and vascular endothelial function in spontaneously hypertensive rats. Journal of Nutritional Science and Vitaminology, 54(1): 95–98. https://doi.org/ 10.3177/jnsv.54.95
30. Yan, M., Wang, Y., Watharkar, R. B., Pu, Y., Wu, C., Lin, M., Lu, D., Liu, M., Bao, J., Xia, Y. (2022). Physicochemical and antioxidant activity of fruit harvested from eight jujube (Ziziphus jujuba Mill.) cultivars at different development stages. Scientific Reports, 12(1). https://doi.org/10.1038/s41598-022-06313-5
31. Yilmaz, M. A. (2020). Simultaneous quantitative screening of 53 phytochemicals in 33 species of medicinal and aromatic plants: A detailed, robust and comprehensive LC–MS/MS method validation. Industrial Crops and Products, 149: 112347. https://doi.org/10.1016/ j.indcrop.2020.112347
32. Yilmaz, M. A., Ertas, A., Yener, I., Akdeniz, M., Cakir, O., Altun, M., Demirtas, I., Boga, M., Temel, H. (2018). A comprehensive LC–MS/MS method validation for the quantitative investigation of 37 fingerprint phytochemicals in Achillea species: A detailed examination of A. coarctata and A. monocephala. Journal of Pharmaceutical and Biomedical Analysis, 154: 413–424. https://doi.org/10.1016/ J.JPBA.2018.02.059
33. Yücetepe, A., Şensu, E., Duran, A., Özçelik, B. (2023). Investigation of changes in some bioactive properties of phenolic extracts from pulp and seed tissues of Ziziphus jujuba during in vitro digestion. Gıda, 48(3): 602–613. https://doi.org/ 10.15237/gida.GD23033
34. Zargoosh, Z., Ghavam, M., Bacchetta, G., Tavili, A. (2019). Effects of ecological factors on the antioxidant potential and total phenol content of Scrophularia striata Boiss. Scientific Reports, 9(1):16021. https://doi.org/10.1038/s41598-019-52605-8
35. Zheng, Y., Li, Y., Zhang, Y., Ruan, X., Zhang, R. (2017). Purification, characterization, synthesis, in vitro ACE inhibition and in vivo antihypertensive activity of bioactive peptides derived from oil palm kernel glutelin-2 hydrolysates. Journal of Functional Foods, 28: 48–58. https://doi.org/ 10.1016/J.JFF.2016.11.021
36. Zhu, J., Lu, Y., He, Q. (2024). Recent advances on bioactive compounds, health benefits, and potential applications of jujube (Ziziphus Jujuba Mill.): A perspective of by-products valorization. Trends in Food Science & Technology, 145: 104368. https://doi.org/10.1016/J.TIFS.2024.104368