DOI QR코드

DOI QR Code

Photoprotective Potential of Penta-O-Galloyl-β-D-Glucose by Targeting NF-κB and MAPK Signaling in UVB Radiation-Induced Human Dermal Fibroblasts and Mouse Skin

  • Kim, Byung-Hak (Department of Pharmacology, Seoul National University College of Medicine) ;
  • Choi, Mi Sun (Department of Herbal Biotechnology, Daegu Haany University) ;
  • Lee, Hyun Gyu (Department of Microbiology and Immunology, Yonsei University College of Medicine) ;
  • Lee, Song-Hee (Department of Pharmacology, Seoul National University College of Medicine) ;
  • Noh, Kum Hee (Department of Pharmacology, Seoul National University College of Medicine) ;
  • Kwon, Sunho (Department of Pharmacology, Seoul National University College of Medicine) ;
  • Jeong, Ae Jin (Department of Pharmacology, Seoul National University College of Medicine) ;
  • Lee, Haeri (Department of Pharmacology, Seoul National University College of Medicine) ;
  • Yi, Eun Hee (Department of Pharmacology, Seoul National University College of Medicine) ;
  • Park, Jung Youl (Industry-Academic Cooperation Foundation, Hanbat National University) ;
  • Lee, Jintae (Department of Cosmeceutical Science, Daegu Haany University) ;
  • Joo, Eun Young (Department of Herbal Biotechnology, Daegu Haany University) ;
  • Ye, Sang-Kyu (Department of Pharmacology, Seoul National University College of Medicine)
  • Received : 2015.06.15
  • Accepted : 2015.09.04
  • Published : 2015.11.30

Abstract

Exposure of the skin to ultraviolet radiation can cause skin damage with various pathological changes including inflammation. In the present study, we identified the skin-protective activity of 1,2,3,4,6-penta-O-galloyl-${\beta}$-D-glucose (pentagalloyl glucose, PGG) in ultraviolet B (UVB) radiation-induced human dermal fibroblasts and mouse skin. PGG exhibited antioxidant activity with regard to intracellular reactive oxygen species (ROS) generation as well as ROS and reactive nitrogen species (RNS) scavenging. Furthermore, PGG exhibited anti-inflammatory activity, inhibiting the activation of nuclear factor-kappaB (NF-${\kappa}B$) and mitogen-activated protein kinase (MAPK) signaling, resulting in inhibition of the expression of pro-inflammatory mediators. Topical application of PGG followed by chronic exposure to UVB radiation in the dorsal skin of hairless mice resulted in a significant decrease in the progression of inflammatory skin damages, leading to inhibited activation of NF-${\kappa}B$ signaling and expression of pro-inflammatory mediators. The present study demonstrated that PGG protected from skin damage induced by UVB radiation, and thus, may be a potential candidate for the prevention of environmental stimuli-induced inflammatory skin damage.

Keywords

References

  1. Alfadda, A.A., and Sallam, R.M. (2012). Reactive oxygen species in health and disease. J. Biomed. Biotechnol. 2012, 936486.
  2. Balavoine, G.G., and Geletii, Y.V. (1999). Peroxynitrite scavenging by different antioxidants. Part I: convenient assay. Nitric Oxide 3, 40-54. https://doi.org/10.1006/niox.1999.0206
  3. Berneburg, M., Plettenberg, H., and Krutmann, J. (2000). Photoaging of human skin. Photodermatol. Photoimmunol. Photomed. 16, 239-244. https://doi.org/10.1034/j.1600-0781.2000.160601.x
  4. Bickers, DR, and Athar M. (2006). Oxidative stress in the pathogenesis of skin disease. J. Invest. Dermatol. 126, 2565-2575. https://doi.org/10.1038/sj.jid.5700340
  5. Binkley, R.C., Ziepfel, J.C., and Himmeldirk, K.B. (2009). Anomeric selectivity in the synthesis of galloyl esters of D-glucose. Carbohydr. Res. 344, 237-239. https://doi.org/10.1016/j.carres.2008.10.024
  6. Bissett, D.L., Chatterjee, R., and Hannon, D.P. (1990). Photoprotective effect of superoxide-scavenging antioxidants against ultraviolet radiation-induced chronic skin damage in the hairless mouse. Photodermatol. Photoimmunol. Photomed. 7, 56-62.
  7. Brieger, K., Schiavone, S., Miller, F.J. Jr., and Krause, K.H. (2012). Reactive oxygen species: from health to disease. Swiss Med. Wkly 142, w13659.
  8. Chen, Y., and Hagerman, A.E. (2004). Characterization of soluble non-covalent complexes between bovine serum albumin and beta-1,2,3,4,6-penta-O-galloyl-D-glucopyranose by MALDI-TOF MS. J. Agric. Food Chem. 52, 4008-4011. https://doi.org/10.1021/jf035536t
  9. Chen, Y., Hagerman, A.E., and Minto, R. (2003). Preparation of 1,2,3,4,6-penta-O-galloyl-[$U-^{14}C$]-D-glucopyranose. J. Labelled Compd. Rad. 46, 99-105.
  10. Diffey, B.L. (1991). Solar ultraviolet radiation effects on biological systems. Phys. Med. Biol. 36, 299-328. https://doi.org/10.1088/0031-9155/36/3/001
  11. Fan, J., Frey, M.S., and Malik, A.B. (2003). TLR4 signaling induces TLR2 expression in endothelial cells via neutrophil NADPH oxidase. J. Clin. Invest. 112, 1234-1243. https://doi.org/10.1172/JCI18696
  12. Farage, M.A., Miller, K.W., Elsner, P., and Maibach, H.I. (2008). Intrinsic and extrinsic factors in skin ageing: a review. Int. J. Cosmet. Sci. 30, 87-95. https://doi.org/10.1111/j.1468-2494.2007.00415.x
  13. Fisher, G.J., Datta, S.C., Talwar, H.S., Wang, Z.Q., Varani, J., Kang, S., and Voorhees, J.J. (1996). Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature 379, 335-339. https://doi.org/10.1038/379335a0
  14. Fisher, G.J., Datta, S., Wang, Z., Li, X.Y., Quan, T., Chung, J.H., Kang, S., and Voorhees, J.J. (2000). c-Jun-dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoic acid. J. Clin. Invest. 106, 663-670. https://doi.org/10.1172/JCI9362
  15. Fu, X.J., Peng, Y.B., Hu, Y.P., Shi, Y.Z., Yao, M., and Zhang, X. (2014). NADPH oxidase 1 and its derived reactive oxygen species mediated tissue injury and repair. Oxid. Med. Cell. Longev. 2014, 282854.
  16. Gilchrest, BA. (2013). Photoaging. J. Invest. Dermatol. 133, E2-E6. https://doi.org/10.1038/skinbio.2013.176
  17. Hofmann, A.S., and Gross, G.G. (1990). Biosynthesis of gallotannins: formation of polygalloylglucoses by enzymatic acylation of 1,2,3,4,6-penta-O-galloylglucose. Arch. Biochem. Biophys. 283, 530-532. https://doi.org/10.1016/0003-9861(90)90678-R
  18. Hockberger, P.E. (2002). A history of ultraviolet photobiology for humans, animals and microorganisms. Photochem. Photobiol. 76, 561-579. https://doi.org/10.1562/0031-8655(2002)076<0561:AHOUPF>2.0.CO;2
  19. Ichihashi, M., Ueda, M., Budiyanto, A., Bito, T., Oka, M., Fukunaga, M., Tsuru, K., and Horikawa, T. (2003). UV-induced skin damage. Toxicology 189, 21-39. https://doi.org/10.1016/S0300-483X(03)00150-1
  20. Jang, S.E., Hyam, S.R., Jeong, J.J., Han, M.J., and Kim, D.H. (2013). Penta-O-galloyl-$\beta$-D-glucose ameliorates inflammation by inhibiting MyD88/NF-$NF-{\kappa}B$ and MyD88/MAPK signalling pathways. Br. J. Pharmacol. 170, 1078-1091. https://doi.org/10.1111/bph.12333
  21. Khanbabaee, K., and Lotzerich, K. (1997). Efficient total synthesis of the natural products 2,3,4,6-tetra-O-galloyl-d-glucopyranose, 1,2,3,4,6-penta-O-galloyl-beta-D-glucopyranose and the unnatural 1,2,3,4,6-penta-O-galloyl-alpha-D-glucopyranose. Tetrahedron 53, 10725-10732. https://doi.org/10.1016/S0040-4020(97)00702-3
  22. Kim, J., Hwang, J.S., Cho, Y.K., Han, Y., Jeon, Y.J., and Yang, K.H. (2001). Protective effects of (-)-epigallocatechin-3-gallate on UVA- and UVB-induced skin damage. Skin Pharmacol. Appl. Skin Physiol. 14, 11-19. https://doi.org/10.1159/000056329
  23. Kim, Y., Kim, B.H., Lee, H., Jeon, B., Lee, Y.S., Kwon, M.J., Kim, T.Y. (2011). Regulation of skin inflammation and angiogenesis by ECSOD via HIF-$1{\alpha}$ and $NF-{\kappa}B$ pathways. Free Radic. Biol. Med. 51, 1985-1995. https://doi.org/10.1016/j.freeradbiomed.2011.08.027
  24. Kim, B.H., Won, C., Lee, Y.H., Choi, J.S., Noh, K.H., Han, S., Lee, H., Lee, C.S., Lee, D.S., Ye, S.K., et al. (2013a). Sophoraflavanone G induces apoptosis of human cancer cells by targeting upstream signals of STATs. Biochem. Pharmacol. 86, 950-959. https://doi.org/10.1016/j.bcp.2013.08.009
  25. Kim, B.H., Na, K.M., Oh, I., Song, I.H., Lee, Y.S., Shin, J., and Kim, T.Y. (2013b). Kurarinone regulates immune responses through regulation of the JAK/STAT and TCR-mediated signaling pathways. Biochem. Pharmacol. 85, 1134-1144. https://doi.org/10.1016/j.bcp.2013.01.005
  26. Kim, B.H., Choi, J.S., Yi, E.H., Lee, J.K., Won, C., Ye, S.K., and Kim, M.H. (2013c). Relative antioxidant activities of quercetin and its structurally related substances and their effects on $NF-{\kappa}B$/CRE/AP-1 signaling in murine macrophages. Mol. Cells 35, 410-420. https://doi.org/10.1007/s10059-013-0031-z
  27. Kim, B.H., Han, S., Lee, H., Park, C.H., Chung, Y.M., Shin, K., Lee, H.G., and Ye, S.K. (2015). Metformin enhances the anti-adipogenic effects of atorvastatin via modulation of STAT3 and TGF-$\beta$/Smad3 signaling. Biochem. Biophys. Res. Commun. 456, 173-178. https://doi.org/10.1016/j.bbrc.2014.11.054
  28. Klotz, L.O., Holbrook, N.J., and Sies, H. (2001). UVA and singlet oxygen as inducers of cutaneous signaling events. Curr. Probl. Dermatol. 29, 95-113.
  29. Kohl, E., Steinbauer, J., Landthaler, M., and Szeimies, R.M. (2011). Skin ageing. J. Eur. Acad. Dermatol. Venereol. 25, 873-884. https://doi.org/10.1111/j.1468-3083.2010.03963.x
  30. Kong X., Thimmulappa, R., Kombairaju, P., and Biswal, S. (2010). NADPH oxidase-dependent reactive oxygen species mediate amplified TLR4 signaling and sepsis-induced motality in Nrf2-deficient mice. J. Immunol. 185, 569-577. https://doi.org/10.4049/jimmunol.0902315
  31. Krutmann, J., Morita, A., and Chung, J.H. (2012). Sun exposure: what molecular photodermatology tells us about its good and bad sides. J. Invest. Dermatol. 132, 976-984. https://doi.org/10.1038/jid.2011.394
  32. Lee, S.J., Lee, I.S., and Mar, W. (2003). Inhibition of inducible nitric oxide synthase and cyclooxygenase-2 activity by 1,2,3,4,6-penta-O-galloyl-beta-D-glucose in murine macrophage cells. Arch. Pharm. Res. 26, 832-839. https://doi.org/10.1007/BF02980029
  33. Lee, E.J., Jeon, M.S., Kim, B.D., Kim, J.H., Kwon, Y.G., Lee, H., Lee, Y.S., Yang, J.H., and Kim, T.Y. (2010). Capsiate inhibits ultraviolet B-induced skin inflammation by inhibiting Src family kinases and epidermal growth factor receptor signaling. Free Radic. Biol. Med. 48, 1133-1143. https://doi.org/10.1016/j.freeradbiomed.2010.01.034
  34. Liu, X., Shi, S., Ye, J., Liu, L., Sun, M., and Wang, C. (2009). Effect of polypeptide from Chlamys farreri on UVB-induced ROS/NF-kappaB/COX-2 activation and apoptosis in HaCaT cells. J. Photochem. Photobiol. B. 96, 109-116. https://doi.org/10.1016/j.jphotobiol.2009.04.010
  35. Matsumoto, M., Sudo, T., Saito, T., Osada, H., and Tsujimoto, M. (2000). Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclstogenesis mediated by receptor activator of NF-kappa B ligand (RANKL). J. Biol. Chem. 275, 31155-31161. https://doi.org/10.1074/jbc.M001229200
  36. Niemetz, R., and Gross, G.G. (2005). Enzymology of gallotannin and ellagitannin biosynthesis. Phytochemistry 66, 2001-2011. https://doi.org/10.1016/j.phytochem.2005.01.009
  37. Oh, G.S., Pae, H.O., Choi, B.M., Lee, H.S., Kim, I.K., Yun, Y.G., Kim, J.D., and Chung, H.T. (2004). Penta-O-galloyl-beta-D-glucose inhibits phorbol myristate acetate-induced interleukin-8 gene expression in human monocytic U937 cells through its inactivation of nuclear factor-kappaB. Int. Immunopharmacol. 4, 377-386. https://doi.org/10.1016/j.intimp.2003.10.010
  38. Pan, M.H., Lin-Shiau, S.Y., Ho, C.T., Lin, J.H., and Lin, J.K. (2000). Suppression of lipopolysaccharide-induced nuclear factor-kappaB activity by theaflavin-3,3'-digallate from black tea and other polyphenols through down-regulation of IkappaB kinase activity in macrophages. Biochem. Pharmacol. 59, 357-367. https://doi.org/10.1016/S0006-2952(99)00335-4
  39. Pandey, K.B., and Rizvi, S.I. (2009). Plant polyphenols as dietary antioxidants in human health and disease. Oxid. Med. Cell. Longev. 2, 270-278. https://doi.org/10.4161/oxim.2.5.9498
  40. Park, L.J., Ju, S.M., Song, H.Y., Lee, J.A., Yang, M.Y., Kang, Y.H., Kwon, H.J., Kim, T.Y., Choi, S.Y., and Park, J. (2006). The enhanced monocyte adhesiveness after UVB exposure requires ROS and NF-kappaB signaling in human keratinocyte. J. Biochem. Mol Biol. 39, 618-625. https://doi.org/10.5483/BMBRep.2006.39.5.618
  41. Park, E., Lee, N.H., Baik, J.S., and Jee, Y. (2008). Elaeocarpus sylvestris modulates gamma-ray-induced immunosuppression in mice: implications in radioprotection. Phytother. Res. 22, 1046-1051. https://doi.org/10.1002/ptr.2430
  42. Siomek, A. (2012). $NF-{\kappa}B$ signaling pathway and free radical impact. Acta. Biochim. Pol. 59, 323-331.
  43. Svobodova, A., Psotova J., and Walterova D. (2003). Natural phenolics in the prevention of UV-induced skin damage. A review. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech. Repub. 147, 137-145. https://doi.org/10.5507/bp.2003.019
  44. Svobodova, A., Walterova, D., and Vostalova, J. (2006). Ultraviolet light induced alteration to the skin. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech. Repub. 150, 25-38. https://doi.org/10.5507/bp.2006.003
  45. Uitto, J. Understanding premature skin aging. (1997). N. Engl. J. Med. 337, 1463-1465. https://doi.org/10.1056/NEJM199711133372011
  46. Wagener F.A., Carels, C.E., and Lundvig, D.M. (2013). Targeting the redox balance in inflammatory skin conditions. Int. J. Mol. Sci. 14, 9126-9167. https://doi.org/10.3390/ijms14059126
  47. Wang, S., Uchi, H., Hayashida, S., Urabe, K., Moroi, Y., and Furue, M. (2009). Differential expression of phosphorylated extracellular signal-regulated kinase 1/2, phosphorylated p38 mitogen-activated protein kinase and nuclear factor-kappaB p105/p50 in chronic inflammatory skin diseases. J. Dermatol. 36, 534-540. https://doi.org/10.1111/j.1346-8138.2009.00696.x
  48. Yaar, M., and Gilchrest, B.A. (2007). Photoageing: mechanism, prevention and therapy. Br. J. Dermatol. 157, 874-887. https://doi.org/10.1111/j.1365-2133.2007.08108.x
  49. Yagura, T., Makita, K., Yamamoto, H., Menck, C.F., and Schuch, A.P. (2011). Biological sensor for solar ultraviolet radiation. Sensors (Basel) 11, 4277-4294. https://doi.org/10.3390/s110404277
  50. Yu, W.S., Jeong, S.J., Kim, J.H., Lee, H.J., Song, H.S., Kim, M.S., Ko, E., Lee, H.J., Khil, J.H., Jang, H.J., et al. (2011). The genome-wide expression profile of 1,2,3,4,6-penta-O-galloyl-$\beta$-D-glucose-treated MDA-MB-231 breast cancer cells: molecular target on cancer metabolism. Mol. Cells 32, 123-132. https://doi.org/10.1007/s10059-011-2254-1
  51. Zhang, J., Li, L., Kim, S.H., Hagerman, A.E., and Lu, J. (2009). Anti-cancer, anti-diabetic and other pharmacologic and biological activities of penta-galloyl-glucose. Pharm. Res. 26, 2066-2080. https://doi.org/10.1007/s11095-009-9932-0

Cited by

  1. Alleviation of collagen-induced arthritis by the benzoxathiole derivative BOT-4-one in mice: Implication of the Th1- and Th17-cell-mediated immune responses vol.110-111, 2016, https://doi.org/10.1016/j.bcp.2016.03.018
  2. Pentagalloylglucose (PGG): A valuable phenolic compound with functional properties vol.37, 2017, https://doi.org/10.1016/j.jff.2017.07.045
  3. 1,2,3,4,6-Penta-O-galloyl-ß-D-glucose, a bioactive compound in Elaeocarpus sylvestris extract, inhibits varicella-zoster virus replication vol.144, 2017, https://doi.org/10.1016/j.antiviral.2017.06.018
  4. Melatonin Alleviates Radiation-Induced Lung Injury via Regulation of miR-30e/NLRP3 Axis vol.2019, pp.1942-0994, 2019, https://doi.org/10.1155/2019/4087298
  5. Salidroside prevents skin carcinogenesis induced by DMBA/TPA in a mouse model through suppression of inflammation and promotion of apoptosis vol.39, pp.6, 2015, https://doi.org/10.3892/or.2018.6381
  6. Penta-1,2,3,4,6- O -Galloyl-β- D -Glucose Inhibits UVB-Induced Photoaging by Targeting PAK1 and JNK1 vol.8, pp.11, 2015, https://doi.org/10.3390/antiox8110561
  7. Mechanism of Pentagalloyl Glucose in Alleviating Fat Accumulation in Caenorhabditis elegans vol.67, pp.51, 2015, https://doi.org/10.1021/acs.jafc.9b06167
  8. Cytoprotective effects of a proprietary red maple leaf extract and its major polyphenol, ginnalin A, against hydrogen peroxide and methylglyoxal induced oxidative stress in human keratinocytes vol.11, pp.6, 2020, https://doi.org/10.1039/d0fo00359j
  9. Current evidence to support the therapeutic potential of flavonoids in oxidative stress-related dermatoses vol.26, pp.1, 2015, https://doi.org/10.1080/13510002.2021.1962094