Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Vitis amurensis Ruprecht root inhibited ${\alpha}$-melanocyte stimulating hormone-induced melanogenesis in B16F10 cells

  • Jin, Kyong-Suk (Blue-Bio Industry Regional Innovation Center, Dong-Eui University) ;
  • Oh, You Na (Blue-Bio Industry Regional Innovation Center, Dong-Eui University) ;
  • Hyun, Sook Kyung (Blue-Bio Industry Regional Innovation Center, Dong-Eui University) ;
  • Kwon, Hyun Ju (Blue-Bio Industry Regional Innovation Center, Dong-Eui University) ;
  • Kim, Byung Woo (Blue-Bio Industry Regional Innovation Center, Dong-Eui University)
  • Received : 2013.11.12
  • Accepted : 2014.06.24
  • Published : 2014.10.01
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Abstract

BACKGROUND/OBJECTIVES: The root of Vitis amurensis Ruprecht, a sort of wild-growing grape, has been used in oriental medicine for treatment of skin ailments; however, its dermatological activity is not sufficiently understood. The aim of this study was to investigate tyrosinase inhibitory and anti-melanogenic activities of V. amurensis Ruprecht root methanol extract (VARM) in B16F10 mouse melanoma cells and to attempt to isolate and identify the active compound issued from VARM. MATERIALS/METHODS: Anti-melanogenic activity of VARM was analyzed in ${\alpha}$-melanocyte stimulating hormone (MSH)-stimulated B16F10 cells through evaluation of antioxidative activity as well as inhibited tyrosinase activity and melanin contents compared with those of kojic acid and arbutin. After anti-melanogenic analysis of VARM, serial fractionation, nuclear magnetic resonance (NMR), and thin layer chromatorgraphy (TLC) were applied for identification of active compounds contained in VARM. RESULTS: VARM significantly inhibited oxidative stress and tyrosinase activity and attenuated ${\alpha}$-MSH-induced melanin production in B16F10 cells. For isolation of active compounds, VARM was fractionated using a series of organic solvents, including dichloromethane ($CH_2Cl_2$), ethyl acetate (EtOAc), and n-butanol (n-BuOH). Among fractions showing anti-melanogenic activity, the CH2Cl2 fraction induced the most potent attenuation of melanogenesis without cytotoxicity and the major compound in the $CH_2Cl_2$ fraction was identified as betulinic acid. Betulinic acid isolated from the $CH_2Cl_2$ fraction of VARM significantly attenuated ${\alpha}$-MSH-induced melanogenesis in a dose dependent manner, which was stronger than that of arbutin used as a positive control. CONCLUSIONS: These results indicate that VARM inhibits oxidative stress, tyrosinase activity, and ${\alpha}$-MSH-induced melanogenesis in B16F10 cells, due primarily to the active compound, betulinic acid, in the $CH_2Cl_2$ fraction.

Keywords

References

  1. Yamaguchi Y, Brenner M, Hearing VJ. The regulation of skin pigmentation. J Biol Chem 2007;282:27557-61. https://doi.org/10.1074/jbc.R700026200
  2. Slominski A, Tobin DJ, Shibahara S, Wortsman J. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev 2004;84:1155-228. https://doi.org/10.1152/physrev.00044.2003
  3. Briganti S, Camera E, Picardo M. Chemical and instrumental approaches to treat hyperpigmentation. Pigment Cell Res 2003;16: 101-10. https://doi.org/10.1034/j.1600-0749.2003.00029.x
  4. Costin GE, Hearing VJ. Human skin pigmentation: melanocytes modulate skin color in response to stress. FASEB J 2007;21:976-94. https://doi.org/10.1096/fj.06-6649rev
  5. Kondo T, Hearing VJ. Update on the regulation of mammalian melanocyte function and skin pigmentation. Expert Rev Dermatol 2011;6:97-108. https://doi.org/10.1586/edm.10.70
  6. Cheli Y, Luciani F, Khaled M, Beuret L, Bille K, Gounon P, Ortonne JP, Bertolotto C, Ballotti R. ${\alpha}$MSH and cyclic AMP elevating agents control melanosome pH through a protein kinase A-independent mechanism. J Biol Chem 2009;284:18699-706. https://doi.org/10.1074/jbc.M109.005819
  7. Passeron T, Namiki T, Passeron HJ, Le Pape E, Hearing VJ. Forskolin protects keratinocytes from UVB-induced apoptosis and increases DNA repair independent of its effects on melanogenesis. J Invest Dermatol 2009;129:162-6. https://doi.org/10.1038/jid.2008.182
  8. Lee J, Jung E, Park J, Jung K, Park E, Kim J, Hong S, Park J, Park S, Lee S, Park D. Glycyrrhizin induces melanogenesis by elevating a cAMP level in b16 melanoma cells. J Invest Dermatol 2005;124: 405-11. https://doi.org/10.1111/j.0022-202X.2004.23606.x
  9. Gibbs S, Murli S, De Boer G, Mulder A, Mommaas AM, Ponec M. Melanosome capping of keratinocytes in pigmented reconstructed epidermis--effect of ultraviolet radiation and 3-isobutyl-1-methylxanthine on melanogenesis. Pigment Cell Res 2000;13:458-66. https://doi.org/10.1034/j.1600-0749.2000.130608.x
  10. Agar N, Young AR. Melanogenesis: a photoprotective response to DNA damage? Mutat Res 2005;571:121-32. https://doi.org/10.1016/j.mrfmmm.2004.11.016
  11. Wen KC, Chang CS, Chien YC, Wang HW, Wu WC, Wu CS, Chiang HM. Tyrosol and its analogues inhibit alpha-melanocyte-stimulating hormone induced melanogenesis. Int J Mol Sci 2013;14:23420-40. https://doi.org/10.3390/ijms141223420
  12. Lee JY, Choi HJ, Chung TW, Kim CH, Jeong HS, Ha KT. Caffeic acid phenethyl ester inhibits alpha-melanocyte stimulating hormoneinduced melanin synthesis through suppressing transactivation activity of microphthalmia-associated transcription factor. J Nat Prod 2013;76:1399-405. https://doi.org/10.1021/np400129z
  13. Eves PC, MacNeil S, Haycock JW. ${\alpha}$-Melanocyte stimulating hormone, inflammation and human melanoma. Peptides 2006;27: 444-52. https://doi.org/10.1016/j.peptides.2005.01.027
  14. Mastore M, Kohler L, Nappi AJ. Production and utilization of hydrogen peroxide associated with melanogenesis and tyrosinasemediated oxidations of DOPA and dopamine. FEBS J 2005;272: 2407-15. https://doi.org/10.1111/j.1742-4658.2005.04661.x
  15. Chaubal VA, Nair SS, Ito S, Wakamatsu K, Mojamdar MV. ${\gamma}$-Glutamyl transpeptidase and its role in melanogenesis: redox reactions and regulation of tyrosinase. Pigment Cell Res 2002;15:420-5. https://doi.org/10.1034/j.1600-0749.2002.02004.x
  16. Ha do T, Kim H, Thuong PT, Ngoc TM, Lee I, Hung ND, Bae K. Antioxidant and lipoxygenase inhibitory activity of oligostilbenes from the leaf and stem of Vitis amurensis. J Ethnopharmacol 2009;125:304-9. https://doi.org/10.1016/j.jep.2009.06.019
  17. Weidner S, Powalka A, Karamac M, Amarowicz R. Extracts of phenolic compounds from seeds of three wild grapevinescomparison of their antioxidant activities and the content of phenolic compounds. Int J Mol Sci 2012;13:3444-57. https://doi.org/10.3390/ijms13033444
  18. Wang JN, Chen YJ, Hano Y, Nomura T, Tan RX. Antioxidant activity of polyphenols from seeds of Vitis amurensis in vitro. Acta Pharmacol Sin 2000;21:633-6.
  19. Jang MH, Piao XL, Kim JM, Kwon SW, Park JH. Inhibition of cholinesterase and amyloid-beta aggregation by resveratrol oligomers from Vitis amurensis. Phytother Res 2008;22:544-9. https://doi.org/10.1002/ptr.2406
  20. Kim JY, Jeong HY, Lee HK, Kim S, Hwang BY, Bae K, Seong YH. Neuroprotection of the leaf and stem of Vitis amurensis and their active compounds against ischemic brain damage in rats and excitotoxicity in cultured neurons. Phytomedicine 2012;19:150-9. https://doi.org/10.1016/j.phymed.2011.06.015
  21. Jeong HY, Kim JY, Lee HK, Ha do T, Song KS, Bae K, Seong YH. Leaf and stem of Vitis amurensis and its active components protect against amyloid beta protein (25-35)-induced neurotoxicity. Arch Pharm Res 2010;33:1655-64. https://doi.org/10.1007/s12272-010-1015-6
  22. Lee EO, Lee HJ, Hwang HS, Ahn KS, Chae C, Kang KS, Lu J, Kim SH. Potent inhibition of Lewis lung cancer growth by heyneanol A from the roots of Vitis amurensis through apoptotic and anti-angiogenic activities. Carcinogenesis 2006;27:2059-69. https://doi.org/10.1093/carcin/bgl055
  23. Kim JA, Kim MR, Kim O, Phuong NT, Yun J, Oh WK, Bae K, Kang KW. Amurensin G inhibits angiogenesis and tumor growth of tamoxifen-resistant breast cancer via Pin1 inhibition. Food Chem Toxicol 2012;50:3625-34. https://doi.org/10.1016/j.fct.2012.07.027
  24. Yim N, Ha do T, Trung TN, Kim JP, Lee S, Na M, Jung H, Kim HS, Kim YH, Bae K. The antimicrobial activity of compounds from the leaf and stem of Vitis amurensis against two oral pathogens. Bioorg Med Chem Lett 2010;20:1165-8. https://doi.org/10.1016/j.bmcl.2009.12.020
  25. Shin TY, Kim SH. Meoruh wine suppresses mast cell-mediated allergic inflammation. Immunopharmacol Immunotoxicol 2011;33: 271-8. https://doi.org/10.3109/08923973.2010.500293
  26. Kim SH, Kwon TK, Shin TY. Antiallergic effects of Vitis amurensis on mast cell-mediated allergy model. Exp Biol Med (Maywood) 2008;233:192-9. https://doi.org/10.3181/0708-RM-222
  27. Zhu L, Zhang Y, Lu J. Phenolic contents and compositions in skins of red wine grape cultivars among various genetic backgrounds and originations. Int J Mol Sci 2012;13:3492-510. https://doi.org/10.3390/ijms13033492
  28. Bak MJ, Jun M, Jeong WS. Procyanidins from wild grape (Vitis amurensis) seeds regulate ARE-mediated enzyme expression via Nrf2 coupled with p38 and PI3K/Akt pathway in HepG2 cells. Int J Mol Sci 2012;13:801-18. https://doi.org/10.3390/ijms13010801
  29. Huang KS, Lin M. Oligostilbenes from the roots of Vitis amurensis. J Asian Nat Prod Res 1999;2:21-8. https://doi.org/10.1080/10286029908039886
  30. Oh WK, Cho KB, Hien TT, Kim TH, Kim HS, Dao TT, Han HK, Kwon SM, Ahn SG, Yoon JH, Kim TH, Kim YG, Kang KW. Amurensin G, a potent natural SIRT1 inhibitor, rescues doxorubicin responsiveness via down-regulation of multidrug resistance 1. Mol Pharmacol 2010;78:855-64. https://doi.org/10.1124/mol.110.065961
  31. Lee EO, Kwon BM, Song GY, Chae CH, Kim HM, Shim IS, Ahn KS, Kim SH. Heyneanol A induces apoptosis via cytochrome c release and caspase activation in human leukemic U937 cells. Life Sci 2004;74:2313-26. https://doi.org/10.1016/j.lfs.2003.10.004
  32. Huang KS, Lin M, Cheng GF. Anti-inflammatory tetramers of resveratrol from the roots of Vitis amurensis and the conformations of the seven-membered ring in some oligostilbenes. Phytochemistry 2001;58:357-62. https://doi.org/10.1016/S0031-9422(01)00224-2
  33. Kedare SB, Singh RP. Genesis and development of DPPH method of antioxidant assay. J Food Sci Technol 2011;48:412-22. https://doi.org/10.1007/s13197-011-0251-1
  34. Piao LZ, Park HR, Park YK, Lee SK, Park JH, Park MK. Mushroom tyrosinase inhibition activity of some chromones. Chem Pharm Bull (Tokyo) 2002;50:309-11. https://doi.org/10.1248/cpb.50.309
  35. Ngamwongsatit P, Banada PP, Panbangred W, Bhunia AK. WST-1- based cell cytotoxicity assay as a substitute for MTT-based assay for rapid detection of toxigenic Bacillus species using CHO cell line. J Microbiol Methods 2008;73:211-5. https://doi.org/10.1016/j.mimet.2008.03.002
  36. Chung KW, Park YJ, Choi YJ, Park MH, Ha YM, Uehara Y, Yoon JH, Chun P, Moon HR, Chung HY. Evaluation of in vitro and in vivo anti-melanogenic activity of a newly synthesized strong tyrosinase inhibitor (E)-3-(2,4 dihydroxybenzylidene)pyrrolidine-2,5-dione (3-DBP). Biochim Biophys Acta 2012;1820:962-9. https://doi.org/10.1016/j.bbagen.2012.03.018
  37. Schwahn DJ, Xu W, Herrin AB, Bales ES, Medrano EE. Tyrosine levels regulate the melanogenic response to alpha-melanocyte-stimulating hormone in human melanocytes: implications for pigmentation and proliferation. Pigment Cell Res 2001;14:32-9. https://doi.org/10.1034/j.1600-0749.2001.140106.x
  38. Park HY, Wu C, Yaar M, Stachur CM, Kosmadaki M, Gilchrest BA. Role of BMP-4 and its signaling pathways in cultured human melanocytes. Int J Cell Biol 2009;2009:750482.
  39. Ding HY, Lin HC, Chang TS. Tyrosinase inhibitors isolated from the roots of Paeonia suffruticosa. J Cosmet Sci 2009;60:347-52.
  40. Zi SX, Ma HJ, Li Y, Liu W, Yang QQ, Zhao G, Lian S. Oligomeric proanthocyanidins from grape seeds effectively inhibit ultravioletinduced melanogenesis of human melanocytes in vitro. Int J Mol Med 2009;23:197-204.
  41. Tan Y, Yu R, Pezzuto JM. Betulinic acid-induced programmed cell death in human melanoma cells involves mitogen-activated protein kinase activation. Clin Cancer Res 2003;9:2866-75.
  42. Chowdhury AR, Mandal S, Mittra B, Sharma S, Mukhopadhyay S, Majumder HK. Betulinic acid, a potent inhibitor of eukaryotic topoisomerase I: identification of the inhibitory step, the major functional group responsible and development of more potent derivatives. Med Sci Monit 2002;8:BR254-65.
  43. Zuco V, Supino R, Righetti SC, Cleris L, Marchesi E, Gambacorti- Passerini C, Formelli F. Selective cytotoxicity of betulinic acid on tumor cell lines, but not on normal cells. Cancer Lett 2002;175:17-25. https://doi.org/10.1016/S0304-3835(01)00718-2
  44. Yogeeswari P, Sriram D. Betulinic acid and its derivatives: a review on their biological properties. Curr Med Chem 2005;12:657-66. https://doi.org/10.2174/0929867053202214
  45. Choi JY, Choi EH, Jung HW, Oh JS, Lee WH, Lee JG, Son JK, Kim Y, Lee SH. Melanogenesis inhibitory compounds from Saussureae radix. Arch Pharm Res 2008;31:294-9. https://doi.org/10.1007/s12272-001-1154-0

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