Korean Journal of Plant Resources (한국자원식물학회지)

The Plant Resources Society of Korea (한국자원식물학회)
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Inhibitory Effects of a Combination of Grapefruit and Rosemary Extracts for Alleviating UV-Induced Skin Ageing

  • Choi, Hee-Jeong (School of Food Science & Biotechnology, Kyungpook National University) ;
  • Alam, Badrul (School of Food Science & Biotechnology, Kyungpook National University) ;
  • Zhao, Peijun (School of Food Science & Biotechnology, Kyungpook National University) ;
  • Cha, Yeong-Ho (School of Food Science & Biotechnology, Kyungpook National University) ;
  • Kim, Tae-Ho (Biomedical Research Institute, Kyungpook National University Hospital) ;
  • Lee, Sang-Han (School of Food Science & Biotechnology, Kyungpook National University)
  • Received : 2019.02.28
  • Accepted : 2019.04.05
  • Published : 2019.06.30
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Abstract

Ultraviolet (UV) radiation is associated with the development of extrinsic skin aging. We performed in vivo assays in order to investigate the protective effect of a combination of grapefruit and rosemary extracts (cG&Re) on UVB-induced skin aging. The results indicated that cG&Re displayed elastase inhibitory activity in a dose-dependent manner. Topical application of cG&Re mitigated photo-aging related lesions such as skin erythema and thickening in photo-aged BALB/c mice dorsal skin, by preventing UVB-induced collagen degradation. Immunohistochemical analyses revealed that cG&Re stimulated SIRT-1 expression, and suppressed MMP-1 and $IL-1{\beta}$ expression. It was observed that expression of MMP-1 and -13 mRNA was downregulated in the cG&Re-treated group. Furthermore, cG&Re treatment drastically suppressed protein expression of MMP-1 and regulated the phosphorylation of p-38 kinase. As expected, oral administration of cG&Re resulted in the same SIRT-1, MMP-1, and $IL-1{\beta}$ expression patterns observed upon topical application of cG&Re in the UV-induced mice model. Overall, the current results demonstrated that cG&Re attenuated both the downregulation of MMP-1 expression and up-regulation of SIRT-1 expression, as well as decreased phosphorylation of MAPK in UVB-induced skin ageing mice model, suggesting that cG&Re might be used as an internal food ingredient for beauty-purposes as well as a functional food material.

Keywords

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Fig. 1. HPLC chromatogram, elastase inhibitory activity and cell vitality of cG&Re.

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Fig. 2. Preventive effects of cG&Re.

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Fig. 3. Effects of cG&Re on histochemical changes and skin aging-related biomarkers.

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Fig. 4. mRNA and protein expression of aging-related biomarkers and signaling molecules induced by cG&Re.

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Fig. 5. Histochemical changes and protein expression of aging-related biomarkers induced by oral administration of cG&Re.

References

  1. Bissett, D., R. Chatterjee and D. Hannon. 1990. Photoprotective effect of superoxide-scavenging antioxidants against ultraviolet radiation-induced chronic skin damage in the hairless mouse. Photodermatol Photo. 7(2):56-62.
  2. Cao, C., S. Lu, R. Kivlin, B. Wallin, E. Card, A. Bagdasarian, T. Tamakloe, W.J. Wang, X. Song and W.M. Chu. 2009. SIRT1 confers protection against UVB-and H2O2-induced cell death via modulation of p53 and JNK in cultured skin keratinocytes. J Cell Mol Med. 13(9b):3632-3643. https://doi.org/10.1111/j.1582-4934.2008.00453.x
  3. Chanda, S. and K. Rakholiya. 2011. Combination therapy: Synergism between natural plant extracts and antibiotics against infectious diseases. Microbiol Book Series:520-529.
  4. Cheung, S. and J. Tai. 2007. Anti-proliferative and antioxidant properties of rosemary Rosmarinus officinalis. Oncol Rep. 17(6):1525-1531.
  5. Choi, S., J. Youn, K. Kim, D.H. Joo, S. Shin, J. Lee, H.K. Lee, I.-S. An, S. Kwon and H.J. Youn. 2016. Apigenin inhibits UVA-induced cytotoxicity in vitro and prevents signs of skin aging in vivo. Int J Mol Med 38(2):627-634. https://doi.org/10.3892/ijmm.2016.2626
  6. Cristobal-Luna, J.M., I. Alvarez-Gonzalez, E. Madrigal-Bujaidar and G. Chamorro-Cevallos. 2018. Grapefruit and its biomedical, antigenotoxic and chemopreventive properties. Food Chem Toxicol 112:224-234. https://doi.org/10.1016/j.fct.2017.12.038
  7. Cuvelier, M.E., H. Richard and C. Berset. 1996. Antioxidative activity and phenolic composition of pilot-plant and commercial extracts of sage and rosemary. J Am Oil Chem Soc 73(5):645-652. https://doi.org/10.1007/BF02518121
  8. D'Orazio, J., S. Jarrett, A. Amaro-Ortiz and T. Scott. 2013. UV radiation and the skin. Int J Mol Sci 14(6):12222-12248. https://doi.org/10.3390/ijms140612222
  9. Erenmemisoglu, A., R. Saraymen and S. Ustun. 1997. Effect of a Rosmarinus officinalis leave extract on plasma glucose levels in normoglycaemic and diabetic mice. Die Pharmazie 52(8): 645.
  10. Fisher, G.J., S. Datta, Z. Wang, X.-Y. Li, T. Quan, J.H. Chung, S. Kang and J.J. Voorhees. 2000. c-Jun-dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoic acid. J Clin Invest 106(5):663-670. https://doi.org/10.1172/JCI9362
  11. Fisher, G.J., T. Quan, T. Purohit, Y. Shao, M.K. Cho, T. He, J. Varani, S. Kang and J.J. Voorhees. 2009. Collagen fragmentation promotes oxidative stress and elevates matrix metalloproteinase-1 in fibroblasts in aged human skin. Am J Pathol 174(1):101-114. https://doi.org/10.2353/ajpath.2009.080599
  12. Fisher, G.J., Z. Wang, S.C. Datta, J. Varani, S. Kang and J.J. Voorhees. 1997. Pathophysiology of premature skin aging induced by ultraviolet light. New Engl J Med 337(20):1419-1429. https://doi.org/10.1056/NEJM199711133372003
  13. Garcia-Martinez, E., I. Andujar, A. Yuste del Carmen, J. Prohens and N. Martinez-Navarrete. 2018. Antioxidant and anti-inflammatory activities of freeze-dried grapefruit phenolics as affected by gum arabic and bamboo fibre addition and microwave pretreatment. J Sci Food Agr 98(8):3076-3083. https://doi.org/10.1002/jsfa.8807
  14. Haigis, M.C. and D.A. Sinclair. 2011. Sirtuins in aging and age-related diseases. Handbook of the biology of aging, Elsevier:243-274.
  15. Hubbard, B.P. and D.A. Sinclair. 2014 Small molecule SIRT1 activators for the treatment of aging and age-related diseases. Trends Pharmacol Sci 35(3):146-154. https://doi.org/10.1016/j.tips.2013.12.004
  16. Inomata, S., K. Takada, M. Tsunenaga, M. Fukuda, Y. Matsunaga, S. Amano, K. Kobayashi, T. Nishiyama and Y. Kohno. 2003. Possible involvement of gelatinases in basement membrane damage and wrinkle formation in chronically ultraviolet B-exposed hairless mouse. J Invest Dermatol 120(1):128-134. https://doi.org/10.1046/j.1523-1747.2003.12021.x
  17. Kang, M., S. Yumnam and S. Kim. 2018. Oral intake of collagen peptide attenuates ultraviolet B irradiation-induced skin dehydration in vivo by regulating hyaluronic acid synthesis. Int J Mol Sci 19(11):3551. https://doi.org/10.3390/ijms19113551
  18. Kaurinovic, B. and D. Vastag. 2019. Flavonoids and Phenolic Acids as Potential Natural Antioxidants. Antioxidants, Intech-Open.
  19. Khan, I. A. and E.A. Abourashed. 2011. Leung's Encyclopedia of Common Natural Ingredients: used in food, drugs and cosmetics, John Wiley & Sons. Emeraldinsight, Hoboken, New Jersy.
  20. Kim, J.-K., Y. Kim, K.-M. Na, Y.-J. Surh and T.-Y. Kim. 2007. Gingerol prevents UVB-induced ROS production and COX-2 expression in vitro and in vivo. Free Radical Research 41(5):603-614. https://doi.org/10.1080/10715760701209896
  21. Koo, H. J., S.R. Lee, Y. Park, J.W. Lee, G. So, S.H. Kim and H. Lim. 2018. Inhibitory effects of ethanol extract from Angelica tenuissima root on oxidative stress and melanogenesis. Korean J. Plant Res. 31(4):312-321 (in Korean). https://doi.org/10.7732/kjpr.2018.31.4.312
  22. Kraunsoe, J.A., T.D. Claridge and G. Lowe. 1996. Inhibition of human leukocyte and porcine pancreatic elastase by homologues of bovine pancreatic trypsin inhibitor. Biochemistry 35(28):9090-9096. https://doi.org/10.1021/bi953013b
  23. Kruger, N.J. 2009. The Bradford Method for Protein Quantitation. The Protein Protocols Handbook, Springer, Totowa, New Jersy, pp. 17-24.
  24. Liu, Y., E. Hwang, H. Ngo, H. Perumalsamy, Y. Kim, L. Li and T.-H. Yi. 2018a. Protective effects of Euphrasia officinalis extract against ultraviolet B-induced photoaging in normal human dermal fibroblasts. Int J Mol Sci 19(11):3327. https://doi.org/10.3390/ijms19113327
  25. McCullough, J. L. and K. M. Kelly. 2006. Prevention and treatment of skin aging. Ann Ny Acad Sci 1067(1):323-331. https://doi.org/10.1196/annals.1354.044
  26. Orjalo, A.V., D. Bhaumik, B.K. Gengler, G.K. Scott and J. Campisi. 2009. Cell surface-bound IL-$1{\alpha}$ is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Pnatla Sci India A 106(40):17031-17036.
  27. Park, J.E., H.B. Pyun, S.W. Woo, J.H. Jeong and J.K. Hwang. 2014. The protective effect of K aempferia parviflora extract on UVB-induced skin photoaging in hairless mice. Photodermatol Photo 30(5):237-245. https://doi.org/10.1111/phpp.12097
  28. Perez-Sanchez, A., E. Barrajon-Catalan, N. Caturla, J. Castillo, O. Benavente-Garcia, M. Alcaraz and V. Micol. 2014. Protective effects of citrus and rosemary extracts on UV-induced damage in skin cell model and human volunteers. J Photochem Photobiol B 136:12-18. https://doi.org/10.1016/j.jphotobiol.2014.04.007
  29. Quan, T., Z. Qin, W. Xia, Y. Shao, J.J. Voorhees and G.J. Fisher. 2009. Matrix-degrading metalloproteinases in photoaging. J Invest Derm Symp p, Elsevier.
  30. Rittie, L. and G. J. Fisher. 2002a. UV-light-induced signal cascades and skin aging. Ageing Res Rev 1(4):705-720. https://doi.org/10.1016/S1568-1637(02)00024-7
  31. Rittie, L. and G. J. Fisher. 2015. Natural and sun-induced aging of human skin. Csh Perspect Med 5(1): a015370.
  32. Rosenthal, F.S., A.E. Bakalian and H.R. Taylor. 1986. The effect of prescription eyewear on ocular exposure to ultraviolet radiation. Am J Public Health 76(10):1216-1220. https://doi.org/10.2105/AJPH.76.10.1216
  33. Sekhon-Loodu, S. and H.P. Rupasinghe. 2019. Evaluation of antioxidant, antidiabetic and antiobesity potential of selected traditional medicinal plants. Frontiers in Nutrition 6:53. https://doi.org/10.3389/fnut.2019.00053
  34. Son, Y., S. Kim, H.-T. Chung and H.-O. Pae. 2013. Reactive oxygen species in the activation of MAP kinases. Method Enzymol, Elsevier, 528:27-48. https://doi.org/10.1016/B978-0-12-405881-1.00002-1
  35. Sun, Y., W.-Z. Liu, T. Liu, X. Feng, N. Yang and H.-F. Zhou. 2015a. Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis. J Recept Sig Transd 35(6):600-604. https://doi.org/10.3109/10799893.2015.1030412
  36. Varani, J., R. L. Warner, M. Gharaee-Kermani, S.H. Phan, S. Kang, J. Chung, Z. Wang, S.C. Datta, G.J. Fisher and J.J. Voorhees. 2000. Vitamin a antagonizes decreased cell growth and elevated collagen-degrading matrix metalloproteinases and stimulates collagen accumulation in naturally aged human skin1. J Invest Dermatol 114(3):480-486. https://doi.org/10.1046/j.1523-1747.2000.00902.x
  37. Vincenti, M.P. and C.E. Brinckerhoff. 2002. Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res Ther 4(3):157. https://doi.org/10.1186/ar401
  38. Vogt, T.M., J. Welsh, W. Stolz, F. Kullmann, B. Jung, M. Landthaler and M. McClelland. 1997. RNA fingerprinting displays UVB-specific disruption of transcriptional control in human melanocytes. Cancer Res 57(16):3554-3561.
  39. Wang, X.-y. and Z.-g. Bl. 2006. UVB-irradiated human keratinocytes and interleukin-$1{\alpha}$ indirectly increase MAP kinase/AP-1 activation and MMP-1 production in UVA-irradiated dermal fibroblasts. Chinese Medical Journal. 119(10):827-831. https://doi.org/10.1097/00029330-200605020-00006
  40. Wen, W., J. Chen, L. Ding, X. Luo, X. Zheng, Q. Dai, Q. Gu, C. Liu, M. Liang and X. Guo. 2018. Astragaloside exerts anti-photoaging effects in UVB-induced premature senescence of rat dermal fibroblasts through enhanced autophagy. Arch Biochem Biophys 657:31-40. https://doi.org/10.1016/j.abb.2018.09.007
  41. Xie, M., D. Zhang, J. R. Dyck, Y. Li, H. Zhang, M. Morishima, D.L. Mann, G.E. Taffet, A. Baldini and D.S. Khoury. 2006. A pivotal role for endogenous TGF-${\beta}$-activated kinase-1 in the LKB1/AMP-activated protein kinase energy-sensor pathway. P Natl A Sci 103(46):17378-17383. https://doi.org/10.1073/pnas.0604708103
  42. Xu, G.-H., I.-J. Ryoo, Y.-H. Kim, S.-J. Choo and I.-D. Yoo. 2009. Free radical scavenging and antielastase activities of flavonoids from the fruits of Thuja orientalis. Arch Pharm Res 32(2): 275-282. https://doi.org/10.1007/s12272-009-1233-y
  43. Zhou, X., S.W. Seto, D. Chang, H. Kiat, V. Razmovski-Naumovski, K. Chan and A. Bensoussan . 2016. Synergistic effects of Chinese herbal medicine: a comprehensive review of methodology and current research. Front Pharmacol 7:201.

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