LIU Lulu, ZHANG Sijin, QIN Shaotong, et al. Isolation and Identification of Condensed Tannins from Ziziphus jujuba Leaves and Their Inhibition Mechanism for Melanogenesis[J]. Science and Technology of Food Industry, 2023, 44(1): 78−86. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2022030247.
Citation: LIU Lulu, ZHANG Sijin, QIN Shaotong, et al. Isolation and Identification of Condensed Tannins from Ziziphus jujuba Leaves and Their Inhibition Mechanism for Melanogenesis[J]. Science and Technology of Food Industry, 2023, 44(1): 78−86. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2022030247.

Isolation and Identification of Condensed Tannins from Ziziphus jujuba Leaves and Their Inhibition Mechanism for Melanogenesis

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  • Received Date: March 20, 2022
  • Available Online: November 02, 2022
  • Objective: To explore the structural characteristics of condensed tannins from Ziziphus jujuba leaves and their effect on tyrosinase and the inhibition mechanism for melanogenesis. Methods: The condensed tannins from Z. jujuba leaves were isolated and purified on the basis of Sephadex LH-20 gel column chromatography, and their structural features were identified by thiolysis coupled with high-performance liquid chromatography-electrospray ionization mass spectrometry (Thiolysis-HPLC-ESI-MS). Besides, the inhibitory mechanism of Z. jujuba leaves condensed tannins on tyrosinase was also systematically investigated by enzyme kinetics, UV-vis absorption and fluorescence spectroscopy. Finally, CCK-8 assay, L-DOPA oxidation assay, NaOH cleavage assay and real-time fluorescence quantitative PCR were employed to probe into the effects of Z. jujuba leaves condensed tannins on the proliferation, tyrosinase activity, melanogenesis and the level of melanogenesis-related gene expression of mouse melanoma cells (B16F10). Results: The condensed tannins from Z. jujuba leaves were mainly composed of (epi)catechin and (epi)gallocatechin. Z. jujuba leaves condensed tannins were found to strongly inhibit on both monophenolase and diphenolase of tyrosinase, and the inhibition against diphenolase was proved to be reversible and mixed-type. It was also observed that the condensed tannins from Z. jujuba leaves could effectively inhibit the cell viability, tyrosinase activity, melanin content, as well as the mRNA expression of TYR, TRP-1 and MITF genes in B16F10 cells. Conclusion: Based on the comprehensive analysis of the biological effects of condensed tannins from Z. jujuba leaves at enzyme level and cell level, we could clarify the molecular inhibition mechanism of Z. jujuba leaves condensed tannins on melanogenesis in B16F10 cells. This study would provide a theoretical basis for the later development of Z. jujuba leaves condensed tannins as new whitening cosmetic additives and preservatives for fruits and vegetables.
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  • [1]
    ZOLGHADRI S, BAHRAMI A, HASSAN KHAN M T, et al. A comprehensive review on tyrosinase inhibitors[J]. Journal of Enzyme Inhibition and Medicinal Chemistry,2019,34(1):279−309. doi: 10.1080/14756366.2018.1545767
    [2]
    KUMARI S, THNG S, VERMA N K, et al. Melanogenesis inhibitors[J]. Acta Dermato-Venereologica,2018,98(10):924−931. doi: 10.2340/00015555-3002
    [3]
    SHAO Y, JIANG Z, ZENG J, et al. Effect of ethanol fumigation on pericarp browning associated with phenol metabolism, storage quality, and antioxidant systems of wampee fruit during cold storage[J]. Food Science and Nutrition,2020,8(7):3380−3388. doi: 10.1002/fsn3.1617
    [4]
    CHAI W M, WEI Q M, DENG W L, et al. Anti-melanogenesis properties of condensed tannins from Vigna angularis seeds with potent antioxidant and DNA damage protection activities[J]. Food and Function,2019,10(1):99−111. doi: 10.1039/C8FO01979G
    [5]
    KIM J H, KIM M R, LEE E S, et al. Inhibitory effects of calycosin isolated from the root of Astragalus membranaceus on melanin biosynthesis[J]. Biological and Pharmaceutical Bulletin,2009,2:264−268.
    [6]
    ZHANG X, HU X, HOU A, et al. Inhibitory effect of 2, 4, 2', 4'-tetrahydroxy-3-(3-methyl-2-butenyl)-chalcone on tyrosinase activity and melanin biosynthesis[J]. Biological and Pharmaceutical Bulletin,2009,32(1):86−90. doi: 10.1248/bpb.32.86
    [7]
    林益明, 向平, 林鹏. 红树林单宁的研究进展[J]. 海洋科学,2005,29:59−63. [LIN Y M, XIANG P, LIN P. Studies on tannins of mangroves-a review[J]. Marine Sciences,2005,29:59−63.
    [8]
    SALMINEN J P. Two-dimensional tannin fingerprints by liquid chromatography tandem mass spectrometry offer a new dimension to plant tannin analyses and help to visualize the tannin diversity in plants[J]. Journal of Agricultural and Food Chemistry,2018,66(35):9162−9171. doi: 10.1021/acs.jafc.8b02115
    [9]
    CHEN X X, LIANG G, CHAI W M, et al. Antioxidant and antityrosinase proanthocyanidins from Polyalthia longifolia leaves[J]. Journal of Bioscience and Bioengineering,2014,118(5):583−587. doi: 10.1016/j.jbiosc.2014.04.015
    [10]
    CHAI W M, WEI M K, WANG R, et al. Avocado proanthocyanidins as a source of tyrosinase inhibitors: Structure characterization, inhibitory activity, and mechanism[J]. Journal of Agricultural and Food Chemistry,2015,63(33):7381−7387. doi: 10.1021/acs.jafc.5b03099
    [11]
    DENG Y T, LIANG G, SHI Y, et al. Condensed tannins from Ficus altissima leaves: Structural, antioxidant, and antityrosinase properties[J]. Process Biochemistry,2016,51(8):1092−1099. doi: 10.1016/j.procbio.2016.04.022
    [12]
    SONG W, ZHU X F, DING X D, et al. Structural features, antioxidant and tyrosinase inhibitory activities of proanthocyanidins in leaves of two tea cultivars[J]. International Journal of Food Properties,2017,20:1348−1358. doi: 10.1080/10942912.2016.1209682
    [13]
    CHEN H, SONG W, SUN K K, et al. Structure elucidation and evaluation of antioxidant and tyrosinase inhibitory effect and mechanism of proanthocyanidins from leaf and fruit of Leucaena leucocephala[J]. Journal of Wood Chemistry and Technology,2018,38(6):430−444. doi: 10.1080/02773813.2018.1533975
    [14]
    TATSUNO T, JINNO M, ARIMA Y, et al. Anti-inflammatory and anti-melanogenic proanthocyanidin oligomers from peanut skin[J]. Biological and Pharmaceutical Bulletin,2012,35(6):909−916. doi: 10.1248/bpb.35.909
    [15]
    傅瑜. 杨梅叶原花色素的结构鉴定以及对黑色素生成和细胞凋亡的作用研究[D]. 杭州: 浙江大学, 2015

    FU Y. Structural elucidation and effect on melanogenesis and apoptosis of proanthocyanidins extracted from Chinese bayberry leaves[D]. Hangzhou: Zhejiang University, 2015.
    [16]
    闫艳, 付彩, 杜晨辉. 酸枣叶的营养成分、保健功能及产品开发研究进展[J]. 食品工业科技,2018,39(20):330−336. [YAN Y, FU C, DU C H. Research progress on nutrient composition, health functions and product development of Ziziphi spinosae folium[J]. Science and Technology of Food Industry,2018,39(20):330−336. doi: 10.13386/j.issn1002-0306.2018.20.056
    [17]
    赵新华, 伊丽楠. 酸枣叶提取物对中枢神经系统作用的实验研究[J]. 时珍国医国药,2009,20(2):463−464. [ZHAO X H, YI L N. Effect of Ziziphus jujube leaf extract on the central nervous system[J]. Lishizhen Medicine and Materia Medica Research,2009,20(2):463−464. doi: 10.3969/j.issn.1008-0805.2009.02.110
    [18]
    ZHANG L, LIU P, LI L, et al. Identification and antioxidant activity of flavonoids extracted from Xinjiang jujube (Ziziphus jujube Mill.) leaves with ultra-high pressure extraction technology[J]. Molecules,2018,24(1):122−136. doi: 10.3390/molecules24010122
    [19]
    王迎进, 闫军, 周俊丽, 等. 酸枣叶多糖抗氧化性研究[J]. 食品研究与开发,2013,34(7):92−94. [WANG Y J, YAN J, ZHOU J L, et al. Study on antioxidant activities of polysaccharides from the leaves of Ziziphus jujuba var.spinosa[J]. Food Research and Development,2013,34(7):92−94.
    [20]
    孙艳. 酸枣叶皂苷的制备及其抗氧化损伤作用的研究[D]. 天津: 天津商业大学, 2019

    SUN Y. Preparation of saponins from sour jujube leaves and its antioxidative damage effect[D]. Tianjin: Tianjin University of Commerce, 2019.
    [21]
    孙艳, 崔旭盛, 刘静, 等. 酸枣叶黄酮的提取工艺优化及其抗秀丽隐杆线虫氧化损伤活性[J]. 食品工业科技,2020,41(8):143−150. [SUN Y, CUI X S, LIU J, et al. Optimization of extraction process of flavonoids from Ziziphus jujuba Mill var.spinosa leaves and its antioxidant damage activity in Caenorhabditis elegans[J]. Science and Technology of Food Industry,2020,41(8):143−150. doi: 10.13386/j.issn1002-0306.2020.08.023
    [22]
    SONG W, LIU L L, REN Y J, et al. Inhibitory effects and molecular mechanism on mushroom tyrosinase by condensed tannins isolation from the fruit of Ziziphus jujuba Mill. var.spinosa (Bunge)Hu ex H. F. Chow[J]. International Journal of Biological Macromolecules,2020,165(Pt B):1813−1821.
    [23]
    CUI Y, LIANG G, HU Y H, et al. Alpha-substituted derivatives of cinnamaldehyde as tyrosinase inhibitors: Inhibitory mechanism and molecular analysis[J]. Journal of Agricultural and Food Chemistry,2015,63(2):716−722. doi: 10.1021/jf505469k
    [24]
    SINGH L R, CHEN Y L, XIE Y, et al. Functionality study of chalcone-hydroxypyridinone hybrids as tyrosinase inhibitors and influence on anti-tyrosinase activity[J]. Journal of Enzyme Inhibition and Medicinal Chemistry,2020,35(1):1562−1567. doi: 10.1080/14756366.2020.1801669
    [25]
    SONG W, ZHAO Y Y, REN Y J, et al. Proanthocyanidins isolated from the leaves of Photinia×fraseri block the cell cycle and induce apoptosis by inhibiting tyrosinase activity in melanoma cells[J]. Food and Function,2021,12(9):3978−3991. doi: 10.1039/D1FO00134E
    [26]
    杨安全, 王菁, 沈玥琦, 等. 珍珠提取物对黑色素细胞酪氨酸酶活性和黑色素合成的影响[J]. 药物生物技术,2018,25(4):312−315. [YANG A Q, WANG J, SHEN Y Q, et al. Effects of pearl extract on the tyrosinase activity and melanogenesis of melanoma cells[J]. Pharmaceutical Biotechnology,2018,25(4):312−315. doi: 10.19526/j.cnki.1005-8915.20180407
    [27]
    CHATATIKUN M, YAMAUCHI T, YAMASAKI K, et al. Anti-melanogenic effect of Croton roxburghii and Croton sublyratus leaves in alpha-MSH stimulated B16F10 cells[J]. Journal of Traditional and Complementary Medicine,2019,9(1):66−72. doi: 10.1016/j.jtcme.2017.12.002
    [28]
    NIKOMATSU L, LEUNG J K, WILLIAMS D, et al. Trizene-based tyrosinase inhibitors identified by chemical genetic screening[J]. Pigment Cell Research,2016,18(6):447−453.
    [29]
    CHAI W M, HUANG Q, LIN M Z, et al. Condensed tannins from longan bark as inhibitor of tyrosinase: Structure, activity, and mechanism[J]. Journal of Agricultural and Food Chemistry,2018,66:908−917. doi: 10.1021/acs.jafc.7b05481
    [30]
    吴颖, 王佳其, 唐文, 等. 蒲公英黄酮对酪氨酸酶的抑制机理[J]. 食品工业,2021,42(6):283−287. [WU Y, WANG J Q, TANG W, et al. Inhibitory effect of tyrosinase on flavonoids from dandelion[J]. The Food Industry,2021,42(6):283−287.
    [31]
    WANG M T, JIANG J, TIAN J H, et al. Inhibitory mechanism of novel allosteric inhibitor, Chinese bayberry (Myrica rubra Sieb. et Zucc.) leaves proanthocyanidins against α-glucosidase[J]. Journal of Functional Foods,2019,56:286−294. doi: 10.1016/j.jff.2019.03.026
    [32]
    CHEN X X, SHI Y, CHAI W M, et al. Condensed tannins from Ficus virens as tyrosinase inhibitors: Structure, inhibitory activity and molecular mechanism[J]. Plos One,2014,9(3):e91809. doi: 10.1371/journal.pone.0091809
    [33]
    MU Y, LI L, HU S Q. Molecular inhibitory mechanism of tricin on tyrosinase[J]. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy,2013,107:235−240. doi: 10.1016/j.saa.2013.01.058
    [34]
    BISWAS R, MUKHERJEE P K, DALAI M K, et al. Tyrosinase inhibitory potential of purpurin in Rubia cordifolia—A bioactivity guided approach[J]. Industrial Crops and Products,2015,74:319−326. doi: 10.1016/j.indcrop.2015.04.066
    [35]
    石嘉怿. 青梅花提取物的酪氨酸酶抑制作用及机理研究[J]. 食品工业科技,2011,32(10):205−211. [SHI J Y. Inbihition effect and mechanism of Prunus mume flowers extracts on tyrosinase[J]. Science and Technology of Food Industry,2011,32(10):205−211. doi: 10.13386/j.issn1002-0306.2011.10.014
    [36]
    LECLERC J, BALLOTTI R, BERTOLOTTO C. Pathways from senescence to melanoma: Focus on MITF sumoylation[J]. Oncogene,2017,36(48):6659−6667. doi: 10.1038/onc.2017.292

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