DOI QR코드

DOI QR Code

Artemisia capillaris Thunb. inhibits melanin synthesis activity via ERK-dependent MITF pathway in B16/F10 melanoma cells

  • Saba, Evelyn (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University) ;
  • Oh, Mi Ju (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University) ;
  • Lee, Yuan Yee (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University) ;
  • Kwak, Dongmi (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University) ;
  • Kim, Suk (Department of Veterinary Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Rhee, Man Hee (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University)
  • Received : 2017.11.30
  • Accepted : 2018.01.25
  • Published : 2018.03.31

Abstract

Genus Artemisia occurs as a hardy plant and has a wide range of culinary and medicinal features. In this study, we aimed to describe the melanin inhibitory activity of one Artemisia species, i.e., Artemisia capillaris Thunb. Ethanol extracts of fermented Artemisia capillaris (Art.EtOH.FT) and non-fermented Artemisia capillaris (Art.EtOH.CT) were tested for their ability to inhibit tyrosinase activity and melanin pigmentation. Both extracts showed dose-dependent inhibition against ${\alpha}$-melanocyte stimulating hormone-stimulated melanin formation and tyrosinase activity, without cytotoxicity. At $100{\mu}g/mL$, both extracts showed greater inhibition than kojic acid, the positive control. Protein expressions of microphthalmia-associated transcription factor (MITF), tyrosinase (TYR), tyrosinase-related protein 1 (TRP-1), and tyrosinase-related protein 2 (TRP-2) at the transcriptional level were determined by using real-time and semi-quantitative polymerase chain reaction. To complete the mechanistic study, presences of upstream elements of MITF, the phosphorylated-extracellular signal-regulated kinase (p-ERK), and phosphorylated-mitogen-activated protein kinase kinase (p-MEK) were confirmed by using western blot analysis. Expressions of p-TYR, p-TRP-1 and p-TRP-2, downstream factors for p-ERK and p-MITF, were translationally inhibited by both extracts. Art.EtOH.FT induced more potent effects than Art.EtOH.CT, especially signal transduction effects. In summary, Artemisia capillaris extracts appear to act as potent hypopigmentation agents.

Keywords

References

  1. Aniya Y, Shimabukuro M, Shimoji M, Kohatsu M, Gyamfi MA, Miyagi C, Kunii D, Takayama F, Egashira T. Antioxidant and hepatoprotective actions of the medicinal herb Artemisia campestris from the Okinawa Islands. Biol Pharm Bull 2000, 23, 309-312. https://doi.org/10.1248/bpb.23.309
  2. Brenner M, Hearing VJ. The protective role of melanin against UV damage in human skin. Photochem Photobiol 2008, 84, 539-549. https://doi.org/10.1111/j.1751-1097.2007.00226.x
  3. Cha JD, Moon SE, Kim HY, Cha IH, Lee KY. Essential oil of Artemisia capillaris induces apoptosis in KB cells via mitochondrial stress and caspase activation mediated by MAPK-stimulated signaling pathway. J Food Sci 2009, 74, T75-81. https://doi.org/10.1111/j.1750-3841.2009.01355.x
  4. Chevallier A. The Encyclopedia of Medicinal Plants. p. 170, Dorling Kindersley, St. Leonards, 1996.
  5. dela Pena IJI, Hong E, Kim HJ, de la Pena JB, Woo TS, Lee YS, Cheong JH. Artemisia capillaris Thunberg produces sedative-hypnotic effects in mice, which are probably mediated through potentiation of the GABAA receptor. Am J Chin Med 2015, 43, 667-679. https://doi.org/10.1142/S0192415X1550041X
  6. Englaro W, Bertolotto C, Busca R, Brunet A, Pages G, Ortonne JP, Ballotti R. Inhibition of the mitogen-activated protein kinase pathway triggers B16 melanoma cell differentiation. J Biol Chem 1998, 273, 9966-9970. https://doi.org/10.1074/jbc.273.16.9966
  7. Han KH, Jeon YJ, Athukorala Y, Choi KD, Kim CJ, Cho JK, Sekikawa M, Fukushima M, Lee CH. A water extract of Artemisia capillaris prevents 2,2'-azobis(2-amidinopropane) dihydrochloride-induced liver damage in rats. J Med Food 2006, 9, 342-347. https://doi.org/10.1089/jmf.2006.9.342
  8. Hemesath TJ, Price ER, Takemoto C, Badalian T, Fisher DE. MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature 1998, 391, 298-301. https://doi.org/10.1038/34681
  9. Hu YH, Liu X, Jia YL, Guo YJ, Wang Q, Chen QX. Inhibitory kinetics of chlorocinnamic acids on mushroom tyrosinase. J Biosci Bioeng 2014, 117, 142-146. https://doi.org/10.1016/j.jbiosc.2013.07.002
  10. Joshi RK. Artemisia capillaris: medicinal uses and future source for commercial uses from western Himalaya of Uttrakhand. Asian J Res Pharm Sci 2013, 3, 137-140.
  11. Kim DS, Hwang ES, Lee JE, Kim SY, Kwon SB, Park KC. Sphingosine-1-phosphate decreases melanin synthesis via sustained ERK activation and subsequent MITF degradation. J Cell Sci 2003, 116, 1699-1706. https://doi.org/10.1242/jcs.00366
  12. Kim DS, Jeong YM, Park IK, Hahn HG, Lee HK, Kwon SB, Jeong JH, Yang SJ, Sohn UD, Park KC. A new 2-imino-1,3-thiazoline derivative, KHG22394, inhibits melanin synthesis in mouse B16 melanoma cells. Biol Pharm Bull 2007, 30, 180-183. https://doi.org/10.1248/bpb.30.180
  13. Kim DS, Kim SY, Park SH, Choi YG, Kwon SB, Kim MK, Na JI, Youn SW, Park KC. Inhibitory effects of 4-nbutylresorcinol on tyrosinase activity and melanin synthesis. Biol Pharm Bull 2005, 28, 2216-2219. https://doi.org/10.1248/bpb.28.2216
  14. Kim HR, Kim H, Jung BJ, You GE, Jang S, Chung DK. Lipoteichoic acid isolated from Lactobacillus plantarum inhibits melanogenesis in B16F10 mouse melanoma cells. Mol Cells 2015, 38, 163-170.
  15. Kim JY, Lee JY, Lee WY, Yi Y, Lim Y. Anti-oxidant property and inhibition of melanin synthesis of eight plant extracts. Korean J Microbiol Biotechnol 2010, 38, 414-419.
  16. Kim YI, Lee JH, Park SW, Choi IH, Friedman SL, Woo HJ, Kim YC. Artemisia capillaris Thunb. inhibits cell growth and induces apoptosis in human hepatic stellate cell line LX2. Orient Pharm Exp Med 2010, 10, 254-262.
  17. Kim YS, Bahn KN, Hah CK, Gang HI, Ha YL. Inhibition of 7,12-dimethylbenz[a]anthracene induced mouse skin carcinogenesis by Artemisia capillaris. J Food Sci 2008, 73, T16-20.
  18. Komiyama K, Takamatsu S, Takahashi Y, Shinose M, Hayashi M, Tanaka H, Iwai Y, Omura S, Imokawa G. New inhibitors of melanogenesis, OH-3984 K1 and K2. I. Taxonomy, fermentation, isolation and biological characteristics. J Antibiot (Tokyo) 1993, 46, 1520-1525. https://doi.org/10.7164/antibiotics.46.1520
  19. Koo HN, Hong SH, Jeong HJ, Lee EH, Kim NG, Choi SD, Ra KW, Kim KS, Kang BK, Kim JJ, Oh JG, Kim HM. Inhibitory effect of Artemisia capillaris on ethanolinduced cytokines (TNF-${\alpha}$, IL-$1{\alpha}$) secretion in Hep G2 cells. Immunopharmacol Immunotoxicol 2002, 24, 441-453. https://doi.org/10.1081/IPH-120014728
  20. Kwon OS, Choi JS, Islam MN, Kim YS, Kim HP. Inhibition of 5-lipoxygenase and skin inflammation by the aerial parts of Artemisia capillaris and its constituents. Arch Pharm Res 2011, 34, 1561-1569. https://doi.org/10.1007/s12272-011-0919-0
  21. Lajis AFB, Hamid M, Ariff AB. Depigmenting effect of kojic acid esters in hyperpigmented B16F1 melanoma cells. J Biomed Biotechnol 2012, 2012, 952452.
  22. Lee HJ, Lee WJ, Chang SE, Lee GY. Hesperidin, a popular antioxidant inhibits melanogenesis via Erk1/2 mediated MITF degradation. Int J Mol Sci 2015, 16, 18384-18395. https://doi.org/10.3390/ijms160818384
  23. Lee MK, Choi GP, Ryu LH, Lee GY, Yu CY, Lee HY. [Enhanced immune activity and cytotoxicity of Artemisia capillaris Thunb. extracts against human cell lines]. Korean J Med Crop Sci 2004, 12, 36-42. Korean.
  24. Liu ZL, Chu SS, Liu QR. Chemical composition and insecticidal activity against Sitophilus zeamais of the essential oils of Artemisia capillaris and Artemisia mongolica. Molecules 2010, 15, 2600-2608. https://doi.org/10.3390/molecules15042600
  25. Masamoto Y, Ando H, Murata Y, Shimoishi Y, Tada M, Takahata K. Mushroom tyrosinase inhibitory activity of esculetin isolated from seeds of Euphorbia lathyris L. Biosci Biotechnol Biochem 2003, 67, 631-634. https://doi.org/10.1271/bbb.67.631
  26. Momtaz S, Mapunya BM, Houghton PJ, Edgerly C, Hussein A, Naidoo S, Lall N. Tyrosinase inhibition by extracts and constituents of Sideroxylon inerme L. stem bark, used in South Africa for skin lightening. J Ethnopharmacol 2008, 119, 507-512. https://doi.org/10.1016/j.jep.2008.06.006
  27. Ohguchi K, Tanaka T, Iliya I, Ito T, Iinuma M, Matsumoto K, Akao Y, Nozawa Y. Gnetol as a potent tyrosinase inhibitor from genus Gnetum. Biosci Biotechnol Biochem 2003, 67, 663-665. https://doi.org/10.1271/bbb.67.663
  28. Roh JS, Han JY, Kim JH, Hwang JK. Inhibitory effects of active compounds isolated from safflower (Carthamus tinctorius L.) seeds for melanogenesis. Biol Pharm Bull 2004, 27, 1976-1978. https://doi.org/10.1248/bpb.27.1976
  29. Saba E, Lee CH, Jeong DH, Lee K, Kim TH, Roh SS, Kim SH, Rhee MH. Fermented rice bran prevents atopic dermatitis in DNCB-treated NC/Nga mice. J Biomed Res 2016, 30, 334-343.
  30. Seo KS, Jeong HJ, Yun KW. Antimicrobial activity and chemical components of two plants, Artemisia capillaris and Artemisia iwayomogi, used as Korean herbal Injin. J Ecol Field Biol 2010, 33, 141-147.
  31. Shen T, Heo SI, Wang MH. Involvement of the p38 MAPK and ERK signaling pathway in the anti-melanogenic effect of methyl 3,5-dicaffeoyl quinate in B16F10 mouse melanoma cells. Chem Biol Interact 2012, 199, 106-111. https://doi.org/10.1016/j.cbi.2012.06.004
  32. Tan RX, Zheng WF, Tang HQ. Biologically active substances from the genus Artemisia. Planta Med 1998, 64, 295-302. https://doi.org/10.1055/s-2006-957438
  33. Uchida R, Ishikawa S, Tomoda H. Inhibition of tyrosinase activity and melanine pigmentation by 2-hydroxytyrosol. Acta Pharm Sin B 2014, 4, 141-145. https://doi.org/10.1016/j.apsb.2013.12.008
  34. Wu M, Hemesath TJ, Takemoto CM, Horstmann MA, Wells AG, Price ER, Fisher DZ, Fisher DE. c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes Dev 2000, 14, 301-312.
  35. Xie W, Zhang J, Ma X, Yang W, Zhou Y, Tang X, Zou Y, Li H, He J, Xie S, Zhao Y, Liu F. Synthesis and biological evaluation of kojic acid derivatives containing 1,2,4-triazole as potent tyrosinase inhibitors. Chem Biol Drug Des 2015, 86, 1087-1092. https://doi.org/10.1111/cbdd.12577
  36. Yokota T, Nishio H, Kubota Y, Mizoguchi M. The inhibitory effect of glabridin from licorice extracts on melanogenesis and inflammation. Pigment Cell Res 1998, 11, 355-361. https://doi.org/10.1111/j.1600-0749.1998.tb00494.x
  37. Yoon HS, Ko HC, Kim SS, Park KJ, An HJ, Choi YH, Kim SJ, Lee NH, Hyun CG. Tangeretin triggers melanogenesis through the activation of melanogenic signaling proteins and sustained extracellular signal-regulated kinase in B16/F10 murine melanoma cells. Nat Prod Commun 2015, 10, 389-392.

Cited by

  1. Anti-Melanogenic Effects of Korean Red Ginseng Oil in an Ultraviolet B-Induced Hairless Mouse Model vol.25, pp.20, 2020, https://doi.org/10.3390/molecules25204755