Inhibitory effects and underlying mechanisms of <em>Artemisia capillaris</em> essential oil on melanogenesis in the B16F10 cell line

Kim,Min Jae; Mohamed,Elsayed A.; Kim,Da Som; Park,Mi-Jin; Ahn,Byoung-Jun; Jeung,Eui-Bae; An,Beum-Soo

doi:10.3892/mmr.2022.12629

Inhibitory effects and underlying mechanisms of Artemisia capillaris essential oil on melanogenesis in the B16F10 cell line

Authors:
- Min Jae Kim
- Elsayed A. Mohamed
- Da Som Kim
- Mi-Jin Park
- Byoung-Jun Ahn
- Eui-Bae Jeung
- Beum-Soo An
View Affiliations

Affiliations: Department of Biomaterials Science (BK21 FOUR Program), College of Natural Resources and Life Science/Life and Industry Convergence Research Institute, Pusan National University, Miryang, Gyeongsangnam‑do 50463, Republic of Korea, Division of Forest Industrial Materials, Department of Forest Products and Industry, National Institute of Forest Science, Seoul 02455, Republic of Korea, Laboratory of Veterinary Biochemistry and Molecular Biology, College of Veterinary Medicine, Chungbuk National University, Cheongju, Chungbuk 28644, Republic of Korea
Published online on: February 4, 2022 https://doi.org/10.3892/mmr.2022.12629
Article Number: 113
Copyright : © Kim et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The present study investigated the anti‑melanogenic activity of 10 essential oils using the B16F10 cell model. Initially, a wide range of concentrations of these essential oils were screened in order to determine their toxicity levels. The assigned non‑toxic concentrations of the tested essential oils were then used to evaluate their effects on melanogenesis. The effects of the essential oils with potent anti‑melanogenic activity on cell proliferation, protection against H₂O₂‑induced cell death and the expression of certain melanogenesis‑related genes, including MITF, tyrosinase, tyrosinase related protein (TRP)‑1 and TRP‑2 were also evaluated. The results revealed that the essential oils extracted from Citrus unshiu, Juniperus chinensis L., Zanthoxylum piperitum and Artemisia capillaris (A. capillaris) inhibited melanogenesis. However, among these four extracts, only A. capillaris extract enhanced cell proliferation, exhibited anti‑H₂O₂ activities and decreased the expression level of TRP‑1. It was demonstrated that A. capillaris extract inhibited melanin synthesis via the downregulation of the TRP‑1 translational level. These essential oil extracts, particularly that of A. capillaris, may thus be used as natural anti‑melanogenic agents for therapeutic purposes and in the cosmetic industry for skin whitening effects with beneficial proliferative properties. However, further studies using in vivo models are required to validate these findings and to examine the effects of these extracts on various molecular pathways.

View Figures

View References

1	Tayarani-Najaran Z, Akaberi M, Vatani M and Emami SA: Evaluation of antioxidant and anti-melanogenic activities of different extracts from aerial parts of Nepeta binaludensis Jamzad in murine melanoma B16F10 cells. Iran J Basic Med Sci. 19:662–669. 2016.PubMed/NCBI
2	Slominski A, Tobin DJ, Shibahara S and Wortsman J: Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev. 84:1155–1228. 2004. View Article : Google Scholar : PubMed/NCBI
3	Slominski A, Zmijewski MA and Pawelek J: L-tyrosine and L-dihydroxyphenylalanine as hormone-like regulators of melanocyte functions. Pigment Cell Melanoma Res. 25:14–27. 2012. View Article : Google Scholar : PubMed/NCBI
4	Wang L, Oh JY, Kim YS, Lee HG, Lee JS and Jeon YJ: Anti-photoaging and anti-melanogenesis effects of fucoidan isolated from Hizikia fusiforme and its underlying mechanisms. Mar Drugs. 18:4272020. View Article : Google Scholar : PubMed/NCBI
5	Rok J, Otręba M, Buszman E and Wrześniok D: Melanin-from melanocyte to keratinocyte, that is how melanin is transported within the skin. Ann Acad Med Siles. 66:60–66. 2012.
6	Slominski A, Wortsman J, Luger T, Paus R and Solomon S: Corticotropin releasing hormone and proopiomelanocortin involvement in the cutaneous response to stress. Physiol Rev. 80:979–1020. 2000. View Article : Google Scholar : PubMed/NCBI
7	Slominski AT, Zmijewski MA, Skobowiat C, Zbytek B, Slominski RM and Steketee JD: Sensing the environment: Regulation of local and global homeostasis by the skin's neuroendocrine system. Adv Anat Embryol Cell Biol. 212:vvii, 1, 115. 2012.PubMed/NCBI
8	Otręba M, Buszman E, Miliński M and Wrześniok D: Hypomelanoses transmitted from generation to generation. Postepy Hig Med Dosw (Online). 68:1081–1090. 2014.(In Polish). View Article : Google Scholar : PubMed/NCBI
9	Otręba M, Miliński M, Buszman E, Wrześniok D and Beberok A: Hereditary hypomelanocytoses: the role of PAX3, SOX10, MITF, SNAI2, KIT, EDN3 and EDNRB genes. Postepy Hig Med Dosw (Online). 67:1109–1118. 2013.(In Polish). View Article : Google Scholar : PubMed/NCBI
10	Goswami P and Sharma HK: Skin hyperpigmentation disorders and use of herbal extracts: A review. Curr Trends Pharm Res. 7:81–104. 2020.
11	Burger P, Landreau A, Azoulay S, Michel T and Fernandez X: Skin whitening cosmetics: Feedback and challenges in the development of natural skin lighteners. Cosmetics. 3:362016. View Article : Google Scholar
12	Pollock S, Taylor S, Oyerinde O, Nurmohamed S, Dlova N, Sarkar R, Galadari H, Manela-Azulay M, Chung HS, Handog E and Kourosh AS: The dark side of skin lightening: An international collaboration and review of a public health issue affecting dermatology. Int J Womens Dermatol. 7:158–164. 2020. View Article : Google Scholar : PubMed/NCBI
13	Cestari TF, Dantas LP and Boza JC: Acquired hyperpigmentations. An Bras Dermatol. 89:11–25. 2014. View Article : Google Scholar : PubMed/NCBI
14	Blaut M, Braune A, Wunderlich S, Sauer P, Schneider H and Glatt H: Mutagenicity of arbutin in mammalian cells after activation by human intestinal bacteria. Food Chem Toxicol. 44:1940–1947. 2006. View Article : Google Scholar : PubMed/NCBI
15	Hwang KS, Yang JY, Lee JY, Lee YR, Kim SS, Kim GR, Chae JS, Ahn JH, Shin DS, Choi TY and Bae MA: A novel anti-melanogenic agent, KDZ-001, inhibits tyrosinase enzymatic activity. J Dermatol Sci. 89:165–171. 2018. View Article : Google Scholar : PubMed/NCBI
16	Saeedi M, Eslamifarb M and Khezri K: Kojic acid applications in cosmetic and pharmaceutical preparations. Biomed Pharmacother. 110:582–593. 2019. View Article : Google Scholar : PubMed/NCBI
17	Lee R, Ko HJ, Kim K, Sohn Y, Min SY, Kim JA, Na D and Yeon JH: Anti-melanogenic effects of extracellular vesicles derived from plant leaves and stems in mouse melanoma cells and human healthy skin. J Extracell Vesicles. 9:17034802019. View Article : Google Scholar : PubMed/NCBI
18	Fong P and Tong HH: In silico prediction of the cosmetic whitening effects of naturally occurring lead compounds. Nat Prod Commun. 7:1287–1294. 2012.PubMed/NCBI
19	Huang HC, Wang HF, Yih KH, Chang LZ and Chang TM: The dual antimelanogenic and antioxidant activities of the essential oil extracted from the leaves of acorus macrospadiceus (Yamamoto) F. N. Wei et Y.K. Li. Evid Based Complement Alternat Med. 2012:7812802012. View Article : Google Scholar : PubMed/NCBI
20	Huang HC, Ho YC, Lim JM, Chang TY, Ho CL and Chang TM: Investigation of the anti-melanogenic and antioxidant characteristics of eucalyptus camaldulensis flower essential oil and determination of its chemical composition. Int J Mol Sci. 16:10470–10490. 2015. View Article : Google Scholar : PubMed/NCBI
21	Wu M, Hemesath TJ, Takemoto CM, Horstmann MA, Wells AG, Price ER, Fisher DZ and Fisher DE: c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes Dev. 14:301–12. 2000. View Article : Google Scholar : PubMed/NCBI
22	Herdwiani W, Soemardji AA and Elfahmi Tan MI: Review of cinnamon as a potent anticancer drug. Asian J Pharma Clin Res. 9:8–13. 2016.
23	Kuo ZK, Lin MW, Lu IH, Yao HJ, Wu HC, Wang CC, Lin SH, Wu SY, Tong TS, Cheng YC, et al: Antiangiogenic and antihepatocellular carcinoma activities of the Juniperus chinensis extract. BMC Complement Altern Med. 16:2772016. View Article : Google Scholar : PubMed/NCBI
24	Chung KS, Cheon SY, Roh SS, Lee M and An HJ: Chemopreventive effect of Aster glehni on inflammation-induced colorectal carcinogenesis in mice. Nutrients. 10:2022018. View Article : Google Scholar : PubMed/NCBI
25	Kim J, Jung KH, Yan HH, Cheon MJ, Kang S, Jin X, Park S, Oh MS and Hong SS: Artemisia capillaris leaves inhibit cell proliferation and induce apoptosis in hepatocellular carcinoma. BMC Complement Altern Med. 18:1472018. View Article : Google Scholar : PubMed/NCBI
26	Kono R, Nomura S, Okuno Y, Kagiya T, Nakamura M, Utsunomiya H and Ueno M: Two Japanese pepper (Zanthoxylum piperitum) fruit-derived compounds attenuate IgE-mediated allergic response in vitro and in vivo via inhibition of mast cell degranulation. Eur J Pharmacol. 885:1734352020. View Article : Google Scholar : PubMed/NCBI
27	Kim SS, Baik JS, Oh TH, Yoon WJ, Lee NH and Hyun CG: Biological activities of Korean Citrus obovoides and Citrus natsudaidai essential oils against acne-inducing bacteria. Biosci Biotechnol Biochem. 72:2507–2513. 2008. View Article : Google Scholar : PubMed/NCBI
28	Kang GJ, Han SC, Yi EJ, Kang HK and Yoo ES: The inhibitory effect of premature Citrus unshiu extract on atopic dermatitis in vitro and in vivo. Toxicol Res. 27:173–180. 2011. View Article : Google Scholar : PubMed/NCBI
29	Choi SY, Ko HC, Ko SY, Hwang JH, Park JG, Kang SH, Han SH, Yun SH and Kim SJ: Correlation between flavonoid content and the NO production inhibitory activity of peel extracts from various citrus fruits. Biol Pharm Bull. 30:772–778. 2007. View Article : Google Scholar : PubMed/NCBI
30	Jin KS, Lee JY, Hyun SK, Kim BW and Kwon HJ: Juniperus chinensis and the functional compounds, cedrol and widdrol, ameliorate α-melanocyte stimulating hormone-induced melanin formation in B16F10 Cells. Food Sci Biotechnol. 24:611–618. 2015. View Article : Google Scholar
31	Jin S, Yun HJ, Jeong HY, Oh YN, Park HJ, Yun SG, Kim BW and Kwon HJ: Widdrol, a sesquiterpene isolated from Juniperus chinensis, inhibits angiogenesis by targeting vascular endothelial growth factor receptor 2 signaling. Oncol Rep. 34:1178–1184. 2015. View Article : Google Scholar : PubMed/NCBI
32	Lee SW, Lim JM, Mohan H, Seralathan KK, Park YJ, Lee JH and Oh BT: Enhanced bioactivity of Zanthoxylum schinifolium fermented extract: Anti-inflammatory, anti-bacterial, and anti-melanogenic activity. J Biosci Bioeng. 129:638–645. 2020. View Article : Google Scholar : PubMed/NCBI
33	Laskin JD, Piccinini L, Engelhardt DL and Weinstein IB: Control of melanin synthesis and secretion by B16/C3 melanoma cells. J Cell Physiol. 113:481–486. 1982. View Article : Google Scholar : PubMed/NCBI
34	Bhatnagar V, Srirangam A and Abburi R: In vitro modulation of proliferation and melanization of melanoma cells by citrate. Mol Cell Biochem. 187:57–65. 1998. View Article : Google Scholar : PubMed/NCBI
35	Jeong CH and Shim KH: Tyrosinase inhibitor isolated from the leaves of Zanthoxylum piperitum. Biosci Biotechnol Biochem. 68:1984–1987. 2004. View Article : Google Scholar : PubMed/NCBI
36	Saba E, Oh MJ, Lee YY, Kwak D, Kim S and Rhee MH: Artemisia capillaris thunb. Inhibits melanin synthesis activity via ERK-dependent MITF pathway in B16/F10 melanoma cells. Korean J Vet Res. 58:1–7. 2018. View Article : Google Scholar
37	Kim JK, Park NH and Hwang JS: Skin lightening effect of the dietary intake of citrus peel extract against UV-induced pigmentation. Nat Prod Commun. 14:1934578X198599792019.
38	Burt S: Essential oils: Their antibacterial properties and potential applications in foods-a review. Int J food Microbiol. 94:223–253. 2004. View Article : Google Scholar : PubMed/NCBI
39	Popa M, Măruțescu L, Oprea E, Bleotu C, Kamerzan C, Chifiriuc MC and Grădișteanu Pircalabioru G: In vitro evaluation of the antimicrobial and immunomodulatory activity of culinary herb essential oils as potential perioceutics. Antibiotics (Basel). 9:4282020. View Article : Google Scholar : PubMed/NCBI
40	Dangkulwanich M and Charaslertrangsi T: Hydrodistillation and antimicrobial properties of lemongrass oil (Cymbopogon citratus, Stapf): An undergraduate laboratory exercise bridging chemistry and microbiology. J Food Sci Educ. 19:41–48. 2020. View Article : Google Scholar
41	Baldea I, Mocan T and Cosgarea R: The role of ultraviolet radiation and tyrosine stimulated melanogenesis in the induction of oxidative stress alterations in fair skin melanocytes. Exp Oncol. 31:200–208. 2009.PubMed/NCBI
42	Kim ES, Park SJ, Goh MJ, Na YJ, Jo DS, Jo YK, Shin JH, Choi ES, Lee HK, Kim JY, et al: Mitochondrial dynamics regulate melanogenesis through proteasomal degradation of MITF via ROS-ERK activation. Pigment Cell Melanoma Res. 27:1051–1062. 2014. View Article : Google Scholar : PubMed/NCBI
43	Hong JH, Lee JW, Park JH and Lee IS: Antioxidative and cytoprotective effects of Artemisia capillaris fractions. Biofactors. 31:43–53. 2007. View Article : Google Scholar : PubMed/NCBI
44	Kim ZH, Hwang JW, Lee JH, Kim H, Lim DS, Kang S, Lee HS and Choi YS: Whitening effect of storage protein 2 from silkworm hemolymph. Adv Biosci Biotechnol. 5:758–767. 2014. View Article : Google Scholar
45	Eberle J, Garbe C, Wang N and Orfanos CE: Incomplete expression of the tyrosinase gene family (tyrosinase, TRP-1, and TRP-2) in human malignant melanoma cells in vitro. Pigment Cell Res. 8:307–313. 1995. View Article : Google Scholar : PubMed/NCBI