DOI QR코드

DOI QR Code

The Polyphenol Chlorogenic Acid Attenuates UVB-mediated Oxidative Stress in Human HaCaT Keratinocytes

  • Cha, Ji Won (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Piao, Mei Jing (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Kim, Ki Cheon (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Yao, Cheng Wen (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Zheng, Jian (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Kim, Seong Min (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Hyun, Chang Lim (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Ahn, Yong Seok (Research Institute of Processing from Jeju Fisher Food, Choung Ryong Fisheries Co., LTD.) ;
  • Hyun, Jin Won (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University)
  • Received : 2014.01.24
  • Accepted : 2014.03.06
  • Published : 2014.03.31

Abstract

We investigated the protective effects of chlorogenic acid (CGA), a polyphenol compound, on oxidative damage induced by UVB exposure on human HaCaT cells. In a cell-free system, CGA scavenged 1,1-diphenyl-2-picrylhydrazyl radicals, superoxide anions, hydroxyl radicals, and intracellular reactive oxygen species (ROS) generated by hydrogen peroxide and ultraviolet B (UVB). Furthermore, CGA absorbed electromagnetic radiation in the UVB range (280-320 nm). UVB exposure resulted in damage to cellular DNA, as demonstrated in a comet assay; pre-treatment of cells with CGA prior to UVB irradiation prevented DNA damage and increased cell viability. Furthermore, CGA pre-treatment prevented or ameliorated apoptosis-related changes in UVB-exposed cells, including the formation of apoptotic bodies, disruption of mitochondrial membrane potential, and alterations in the levels of the apoptosis-related proteins Bcl-2, Bax, and caspase-3. Our findings suggest that CGA protects cells from oxidative stress induced by UVB radiation.

Keywords

References

  1. Afaq, F., Adhami, V. M. and Mukhtar, H. (2005) Photochemoprevention of ultraviolet B signaling and photocarcinogenesis. Mutat. Res. 571, 153-173. https://doi.org/10.1016/j.mrfmmm.2004.07.019
  2. Ames, B. N., Shigenaga, M. K. and Hagen, T. M. (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U.S.A. 90, 7915-7922. https://doi.org/10.1073/pnas.90.17.7915
  3. Bowden, G. T. (2004) Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nat. Rev. Cancer 4, 23-35. https://doi.org/10.1038/nrc1253
  4. Caddeo, C., Teskac, K., Sinico, C. and Kristl, J. (2008) Effect of resveratrol incorporated in liposomes on proliferation and UV-B protection of cells. Int. J. Pharm. 363, 183-191. https://doi.org/10.1016/j.ijpharm.2008.07.024
  5. Campanini, M. Z., Pinho-Ribeiro, F. A., Ivan, A. L., Ferreira, V. S., Vilela, F. M., Vicentini, F. T., Martinez, R. M., Zarpelon, A. C., Fonseca, M. J., Faria, T. J., Baracat, M. M., Verri, W. A., Georgetti, S. R. and Casagrande, R. (2013) Efficacy of topical formulations containing Pimenta pseudocaryophyllus extract against UVB-induced oxidative stress and inflammation in hairless mice. J. Photochem. Photobiol. B 127, 153-160. https://doi.org/10.1016/j.jphotobiol.2013.08.007
  6. Carmichael, J., DeGraff, W. G., Gazdar, A. F., Minna, J. D. and Mitchell, J. B. (1987) Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res. 47, 936-942.
  7. Dhumrongvaraporn, A. and Chanvorachote, P. (2013) Kinetics of ultraviolet B irradiation-mediated reactive oxygen species generation in human keratinocytes. J. Cosmet. Sci. 64, 207-217.
  8. Feng, R., Lu. Y., Bowman, L. L., Qian, Y., Castrannova, V. and Ding, M. (2005) Inhibition of activator protein-1, NF-${\kappa}B$, and MAPKs and induction of phase 2 detoxifying enzyme activity by chlorogenic acid. J. Biol. Chem. 280, 27888-27895. https://doi.org/10.1074/jbc.M503347200
  9. Fiorentino, A., D'Abrosca, B., Pacifico, S., Mastellone, C., Piscopo, V., Caputo, R. and Monaco, P. (2008) Isolation and structure elucidation of antioxidant polyphenols from quince (Cydonia vulgaris) peels. J. Agric. Food Chem. 56, 2660-2667. https://doi.org/10.1021/jf800059r
  10. F'Guyer, S., Afaq, F. and Mukhtar, H. (2003) Photochemoprevention of skin cancer by botanical agents. Photodermatol. Photoimmunol. Photomed. 19, 56-72. https://doi.org/10.1034/j.1600-0781.2003.00019.x
  11. Green, D. R. and Reed, J. C. (1998) Mitochondria and apoptosis. Science 281, 1309-1312. https://doi.org/10.1126/science.281.5381.1309
  12. Halliday, G. M. (2005) Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat. Res. 571, 107-120. https://doi.org/10.1016/j.mrfmmm.2004.09.013
  13. Jin, G. H., Liu, Y., Jin, S. Z., Liu, X. D. and Liu, S. Z. (2007) UVB induced oxidative stress in human keratinocytes and protective effect of antioxidant agents. Radiat. Environ. Biophys. 46, 61-68. https://doi.org/10.1007/s00411-007-0096-1
  14. Jost, M., Gasparro, F. P., Jensen, P. J. and Rodeck, U. (2001) Keratinocyte apoptosis induced by ultraviolet B radiation and CD95 ligation - differential protection through epidermal growth factor receptor activation and Bcl-xL expression. J. Invest. Dermatol. 116, 860-866. https://doi.org/10.1046/j.1523-1747.2001.01356.x
  15. Karol, M. H. (2009) How environmental agents influence the aging process. Biomol. Ther. 17, 113-124. https://doi.org/10.4062/biomolther.2009.17.2.113
  16. Kiehne, A. and Engelhardt, U. H. (1996) Thermospray-LC-MS analysis of various groups of polyphenols in tea. II: Chlorogenic acids, theaflavins and thearubigins. Z. Lebensm. Unters. Forsch. 202, 299-302. https://doi.org/10.1007/BF01206100
  17. Kitagawa, S., Yoshii, K., Morita, S. and Teraoka, R. (2011) Efficient topical delivery of chlorogenic acid by an oil-in-water microemulsion to protect skin against UV-induced skin damage. Chem. Pharm. Bull. 59, 793-796. https://doi.org/10.1248/cpb.59.793
  18. Lee, C. W., Ko, H. H., Lin, C. C., Chai, C. Y., Chen, W. T. and Yen, F. L. (2013) Artocarpin attenuates ultraviolet B-induced skin damage in hairless mice by antioxidant and anti-inflammatory effect. Food Chem. Toxicol. 60, 123-129. https://doi.org/10.1016/j.fct.2013.07.029
  19. Lee, E. J., Kim, J. S., Kim, H. P., Lee J. and Kang, S. S. (2010) Phenolic constituents from the flower buds of Lonicera japonica and their 5-lipoxygenase inhibitory activities. Food Chem. 120, 134-139. https://doi.org/10.1016/j.foodchem.2009.09.088
  20. Li, L., Abe, Y., Mashino, T., Mochizuki, M. and Miyata, N. (2003) Signal enhancement in ESR spin-trapping for hydroxyl radicals. Anal. Sci. 19, 1083-1084. https://doi.org/10.2116/analsci.19.1083
  21. Li, L., Abe, Y., Kanagawa, K., Usui, N., Imai, K., Mashino, T., Mochizuki, M. and Miyata, N. (2004) Distinguishing the 5,5-dimethyl-1-pyrroline N-oxide (DMPO)-OH radical quenching effect from the hydroxyl radical scavenging effect in the ESR spin-trapping method. Anal. Chim. Acta 512, 121-124. https://doi.org/10.1016/j.aca.2004.02.020
  22. Li, S., Bian, H., Liu, Z., Wang, Y., Dai, J., He, W., Liao, X., Liu, R. and Luo, J. (2012) Chlorogenic acid protects MSCs against oxidative stress by altering FOXO family genes and activating intrinsic pathway. Eur. J. Pharmacol. 674, 65-72. https://doi.org/10.1016/j.ejphar.2011.06.033
  23. Matsumura, Y. and Ananthaswamy, H. N. (2004) Toxic effects of ultraviolet radiation on the skin. Toxicol. Appl. Pharmacol. 195, 298-308. https://doi.org/10.1016/j.taap.2003.08.019
  24. Mayne, S. T. (2003) Antioxidant nutrients and chronic disease: use of biomarkers of exposureand oxidative stress status in epidemiologic research. J. Nutr. 133, 933S-940S.
  25. McVean, M. and Liebler, D. C. (1999) Prevention of DNA photodamage by vitamin E compounds and sunscreens: roles of ultraviolet absorbance and cellular uptake. Mol. Carcinog. 24, 169-176. https://doi.org/10.1002/(SICI)1098-2744(199903)24:3<169::AID-MC3>3.0.CO;2-A
  26. Morel, Y. and Barouki, R. (1999) Repression of gene expression by oxidative stress. Biochem. J. 342, 481-496. https://doi.org/10.1042/0264-6021:3420481
  27. Narayanan, D. L., Saladi, R. N. and Fox, J. L. (2010) Ultraviolet radiation and skin cancer. Int. J. Dermatol. 49, 978-986. https://doi.org/10.1111/j.1365-4632.2010.04474.x
  28. Paganga, G., Miller, N. and Rice-Evans, C. A. (1999) The polyphenolic content of fruit and vegetables and their antioxidant activities. What does a serving constitute? Free Radic. Res. 30, 153-162. https://doi.org/10.1080/10715769900300161
  29. Park, H. M., Kim, H. J., Jang, Y. P. and Kim, S. Y. (2013) Direct analysis in real time mass spectrometry (DART-MS) analysis of skin metabolome changes in the ultraviolet B-induced mice. Biomol.Ther. 21, 470-475. https://doi.org/10.4062/biomolther.2013.071
  30. Rajagopalan, R., Ranjan, S. K. and Nair, C. K. (2003) Effect of vinblastine sulfate on gamma-radiation-induced DNA single-strand breaks in murine tissues. Mutat. Res. 536, 15-25. https://doi.org/10.1016/S1383-5718(03)00015-9
  31. Rajnochova Svobodova, A. R., Galandakova, A., Palikova, I., Dolezal, D., Kylarova, D., Ulrichova, J. and Vostalova, J. (2013) Effects of oral administration of Lonicera caerulea berries on UVB-induced damage in SKH-1 mice. A pilot study. Photochem. Photobiol. Sci. 12, 1830-1840. https://doi.org/10.1039/c3pp50120e
  32. Rice-Evans, C. A., Miller, N. J. and Paganga, G. (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 20, 933-956. https://doi.org/10.1016/0891-5849(95)02227-9
  33. Rosenkranz, A. R., Schmaldienst, S., Stuhlmeier, K. M., Chen, W., Knapp, W. and Zlabinger, G. J. (1992) A microplate assay for the detection of oxidative products using 2',7'-dichlorofluorescin-diacetate. J. Immunol. Methods 156, 39-45. https://doi.org/10.1016/0022-1759(92)90008-H
  34. Ryter, S. W., Kim, H. P., Hoetzel, A., Park, J. W., Nakahira, K., Wang, X. and Choi, A. M. (2007) Mechanisms of cell death in oxidative stress. Antioxid. Redox Signal. 9, 49-89. https://doi.org/10.1089/ars.2007.9.49
  35. Salucci, S., Burattini, S., Battistelli, M., Baldassarri, V., Maltarello, M. C. and Falcieri, E. (2012) Ultraviolet B (UVB) irradiation-induced apoptosis in various cell lineages in vitro. Int. J. Mol. Sci. 14, 532-546. https://doi.org/10.3390/ijms14010532
  36. Sime, S. and Reeve, V. E. (2004) Protection from inflammation, immunosuppression and carcinogenesis induced by UV radiation in mice by topical Pycnogenol$^{(R)}$. Photochem. Photobiol. 79, 193-198. https://doi.org/10.1562/0031-8655(2004)079<0193:PFIIAC>2.0.CO;2
  37. Singh, N. P. (2000) Microgels for estimation of DNA strand breaks, DNA protein crosslinks and apoptosis. Mutat. Res., 455, 111-127. https://doi.org/10.1016/S0027-5107(00)00075-0
  38. Sklar, L. R., Almutawa, F., Lim, H. W. and Hamzavi, I. (2013) Effects of ultraviolet radiation, visible light, and infrared radiation on erythema and pigmentation: a review. Photochem. Photobiol. Sci. 12, 54-64. https://doi.org/10.1039/C2PP25152C
  39. Susin, S. A., Zamzami, N. and Kroemer, G. (1998) Mitochondria as regulators of apoptosis: doubt no more. Biochim. Biophys. Acta 1366, 151-165. https://doi.org/10.1016/S0005-2728(98)00110-8
  40. Troiano, L., Ferraresi, R., Lugli, E., Nemes, E., Roat, E., Nasi, M., Pinti, M. and Cossarizza, A. (2007) Multiparametric analysis of cells with different mitochondrial membrane potential during apoptosis by polychromatic flow cytometry. Nat. Protoc. 2, 2719-2727. https://doi.org/10.1038/nprot.2007.405
  41. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T., Mazur, M. and Telser, J. (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell. Biol. 39, 44-84. https://doi.org/10.1016/j.biocel.2006.07.001
  42. Vayalil, P. K., Elmets, C. A. and Katiyar, S. K. (2003) Treatment of green tea polyphenols in hydrophilic cream prevents UVB-induced oxidation of lipids and proteins, depletion of antioxidant enzymes and phosphorylation of MAPK proteins in SKH-1 hairless mouse skin. Carcinogenesis 24, 927-936. https://doi.org/10.1093/carcin/bgg025
  43. Vogt, T. M., Welsh, J., Stolz, W., Kullmann, F., Jung, B., Landthaler, M. and McClelland, M. (1997) RNA fingerprinting displays UVB-specific disruption of transcriptional control in human melanocytes. Cancer Res. 57, 3554-3561.
  44. Wen, J., Kang, L., Liu, H., Xiao, Y., Zhang, X. and Chen, Y. (2012) A validated UV-HPLC method for determination of chlorogenic acid in Lepidogrammitis drymoglossoides (Baker) Ching, Polypodiaceae. Pharmacognosy Res. 4, 148-153. https://doi.org/10.4103/0974-8490.99076
  45. Wu, L. (2007) Effect of chlorogenic acid on antioxidant activity of Flos Lonicerae extracts. J. Zhejiang Univ. Sci. B 8, 673-679. https://doi.org/10.1631/jzus.2007.B0673
  46. Zamzami, N., Marchetti, P., Castedo, M., Decaudin, D., Macho, A., Hirsch, T., Susin, S. A., Petit, P. X., Mignotte, B. and Kroemer, G. (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182, 367-377. https://doi.org/10.1084/jem.182.2.367
  47. Zamzami, N., Susin, S. A., Marchetti, P., Hirsch, T., Gomez-Monterrey I., Castedo M. and Kroemer G. (1996) Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183, 1533-1544. https://doi.org/10.1084/jem.183.4.1533

Cited by

  1. Comparison of the antioxidant activities of roasted and explosive puffed coffees vol.52, pp.6, 2017, https://doi.org/10.1111/ijfs.13402
  2. Caffeic Acid Inhibits UVB-induced Inflammation and Photocarcinogenesis Through Activation of Peroxisome Proliferator-activated Receptor-γin Mouse Skin vol.91, pp.6, 2015, https://doi.org/10.1111/php.12522
  3. Role of Chlorogenic Acids in Controlling Oxidative and Inflammatory Stress Conditions vol.8, pp.1, 2015, https://doi.org/10.3390/nu8010016
  4. The antioxidative and cytoprotective effect of Lonicerae japonicae Flos water extracts on the ultraviolet(UV)B-induced human HaCaT keratinocytes vol.29, pp.6, 2014, https://doi.org/10.6116/kjh.2014.29.6.63.
  5. Taste-Masking Effect of Chlorogenic Acid (CGA) on Bitter Drugs Evaluated by Taste Sensor and Surface Plasmon Resonance on the Basis of CGA–Drug Interactions vol.65, pp.2, 2017, https://doi.org/10.1248/cpb.c16-00621
  6. Phenolics from the Patagonian currants Ribes spp.: Isolation, characterization and cytoprotective effect in human AGS cells vol.26, 2016, https://doi.org/10.1016/j.jff.2016.06.036
  7. Non-thermal dielectric-barrier discharge plasma damages human keratinocytes by inducing oxidative stress vol.37, pp.1, 2016, https://doi.org/10.3892/ijmm.2015.2405
  8. Polyphenols as active ingredients for cosmetic products vol.37, pp.5, 2015, https://doi.org/10.1111/ics.12218
  9. Strawberry-Based Cosmetic Formulations Protect Human Dermal Fibroblasts against UVA-Induced Damage vol.9, pp.6, 2017, https://doi.org/10.3390/nu9060605
  10. Antioxidant Property of Coffee Components: Assessment of Methods that Define Mechanisms of Action vol.19, pp.11, 2014, https://doi.org/10.3390/molecules191119180
  11. Alterations of hepatocyte function with free radical generators and reparation or prevention with coffee polyphenols vol.51, pp.3, 2017, https://doi.org/10.1080/10715762.2017.1307979
  12. Protective effect of polysaccharides from Sargassum fusiforme against UVB-induced oxidative stress in HaCaT human keratinocytes vol.36, 2017, https://doi.org/10.1016/j.jff.2017.06.051
  13. Protective Effects of Chlorogenic Acid against Experimental Reflux Esophagitis in Rats vol.22, pp.5, 2014, https://doi.org/10.4062/biomolther.2014.066
  14. Polyphenols and DNA Damage: A Mixed Blessing vol.8, pp.12, 2016, https://doi.org/10.3390/nu8120785
  15. Effect of Thai banana ( Musa AA group) in reducing accumulation of oxidation end products in UVB-irradiated mouse skin vol.168, 2017, https://doi.org/10.1016/j.jphotobiol.2017.01.025
  16. Fractionated Trapa japonica Extracts Inhibit ROS-induced Skin Inflammation in HaCaT keratinocytes vol.41, pp.1, 2015, https://doi.org/10.15230/SCSK.2015.41.1.45
  17. Anti-psoriatic potential of Solanum xanthocarpum stem in Imiquimod-induced psoriatic mice model vol.198, 2017, https://doi.org/10.1016/j.jep.2016.12.046
  18. Chlorogenic acid prevents isoproterenol-induced DNA damage in vascular smooth muscle cells vol.14, pp.5, 2016, https://doi.org/10.3892/mmr.2016.5743
  19. The Study of Anti-/Pro-Oxidant, Lipophilic, Microbial and Spectroscopic Properties of New Alkali Metal Salts of 5-O-Caffeoylquinic Acid vol.19, pp.2, 2018, https://doi.org/10.3390/ijms19020463
  20. Persea americana Mill. crude extract exhibits antinociceptive effect on UVB radiation-induced skin injury in mice pp.1568-5608, 2018, https://doi.org/10.1007/s10787-018-0441-9
  21. ) polyphenol extract against UVB-induced skin damage by modulating the p53 mitochondrial pathway in vitro and in vivo pp.01458884, 2018, https://doi.org/10.1111/jfbc.12708
  22. Silica/Polyethylene Glycol Hybrid Materials Prepared by a Sol-Gel Method and Containing Chlorogenic Acid vol.23, pp.10, 2018, https://doi.org/10.3390/molecules23102447
  23. Consumption of Chlorogenic Acids through Coffee and Health Implications vol.5, pp.1, 2019, https://doi.org/10.3390/beverages5010011
  24. 잔대(Adenophora triphylla var. japonica)순 아세트산에틸 분획물의 피부 미백 효과 vol.30, pp.4, 2014, https://doi.org/10.7732/kjpr.2017.30.4.352
  25. Hawthorn Polyphenol Extract Inhibits UVB-Induced Skin Photoaging by Regulating MMP Expression and Type I Procollagen Production in Mice vol.66, pp.32, 2014, https://doi.org/10.1021/acs.jafc.8b02785
  26. Amelioration of Oxidative Stress in Caco-2 Cells Treated with Pro-inflammatory Proteins by Chlorogenic Acid Isomers via Activation of the Nrf2-Keap1-ARE-Signaling Pathway vol.66, pp.42, 2014, https://doi.org/10.1021/acs.jafc.8b03983
  27. Preparation, structure identification and the anti-photoaging activity of peptide fraction OP-Ia from Ostrea rivularis vol.9, pp.1, 2019, https://doi.org/10.1039/c8ra08137a
  28. 7,8-Dihydroxyflavone Protects High Glucose-Damaged Neuronal Cells against Oxidative Stress vol.27, pp.1, 2014, https://doi.org/10.4062/biomolther.2018.202
  29. Purpurogallin Protects Keratinocytes from Damage and Apoptosis Induced by Ultraviolet B Radiation and Particulate Matter 2.5 vol.27, pp.4, 2014, https://doi.org/10.4062/biomolther.2018.151
  30. Protective Effects and Mechanisms of Pourthiaea villosa (Thunb.) Decne. Extract on Hydrogen Peroxide-Induced Skin Aging in Human Dermal Fibroblasts vol.22, pp.8, 2014, https://doi.org/10.1089/jmf.2018.4379
  31. Carbon Monoxide Partially Mediates Protective Effect of Resveratrol Against UVB-Induced Oxidative Stress in Human Keratinocytes vol.8, pp.10, 2014, https://doi.org/10.3390/antiox8100432
  32. Phenolic and Anthocyanin Compounds and Antioxidant Activity of Tamarillo ( Solanum betaceum Cav.) vol.9, pp.2, 2014, https://doi.org/10.3390/antiox9020169
  33. Topical Application of Aronia melanocarpa Extract Rich in Chlorogenic Acid and Rutin Reduces UVB-Induced Skin Damage via Attenuating Collagen Disruption in Mice vol.25, pp.19, 2020, https://doi.org/10.3390/molecules25194577
  34. Quantification of Chlorogenic Acid and Vanillin from Coffee Peel Extract and its Effect on α-Amylase Activity, Immunoregulation, Mitochondrial Oxidative Stress, and Tumor Suppressor Gene Express vol.12, pp.None, 2014, https://doi.org/10.3389/fphar.2021.760242
  35. Diltiazem-loaded electrospun nanofibers as a new wound dressing: fabrication, characterization, and experimental wound healing vol.26, pp.2, 2014, https://doi.org/10.1080/10837450.2020.1852420
  36. Olive Tree in Circular Economy as a Source of Secondary Metabolites Active for Human and Animal Health Beyond Oxidative Stress and Inflammation vol.26, pp.4, 2014, https://doi.org/10.3390/molecules26041072
  37. Protective Effect of Pyrus ussuriensis Maxim. Extract against Ethanol-Induced Gastritis in Rats vol.10, pp.3, 2021, https://doi.org/10.3390/antiox10030439
  38. Synthesis, Structural, Morphological and Thermal Characterization of Five Different Silica-Polyethylene Glycol-Chlorogenic Acid Hybrid Materials vol.13, pp.10, 2014, https://doi.org/10.3390/polym13101586
  39. Potential Use of Amla (Phyllanthus emblica L.) Fruit Extract to Protect Skin Keratinocytes from Inflammation and Apoptosis after UVB Irradiation vol.10, pp.5, 2021, https://doi.org/10.3390/antiox10050703
  40. Electrospun fibers loaded with Cordia myxa L. fruit extract: Fabrication, characterization, biocompatibility and efficacy in wound healing vol.63, pp.None, 2014, https://doi.org/10.1016/j.jddst.2021.102528
  41. Current State of Knowledge on the Antioxidant Effects and Mechanisms of Action of Polyphenolic Compounds vol.16, pp.7, 2014, https://doi.org/10.1177/1934578x211027745
  42. Phenolic Extract from Aralia nudicaulis L. Rhizomes Inhibits Cellular Oxidative Stresses vol.26, pp.15, 2014, https://doi.org/10.3390/molecules26154458
  43. Beta vulgaris rubra L. (Beetroot) Peel Methanol Extract Reduces Oxidative Stress and Stimulates Cell Proliferation via Increasing VEGF Expression in H2O2 Induced Oxidative Stressed Human Umbilical Vei vol.12, pp.9, 2014, https://doi.org/10.3390/genes12091380
  44. The Analysis of Chlorogenic Acid and Caffeine Content and Its Correlation with Coffee Bean Color under Different Roasting Degree and Sources of Coffee (Coffea arabica Typica) vol.9, pp.11, 2014, https://doi.org/10.3390/pr9112040
  45. Anemopsis californica Attenuates Photoaging by Regulating MAPK, NRF2, and NFATc1 Signaling Pathways vol.10, pp.12, 2014, https://doi.org/10.3390/antiox10121882
  46. Tea and coffee polyphenols and their biological properties based on the latest in vitro investigations vol.175, pp.None, 2014, https://doi.org/10.1016/j.indcrop.2021.114265