Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Padina boryana, a brown alga from the Maldives: inhibition of α-MSH-stimulated melanogenesis via the activation of ERK in B16F10 cells

  • Jayawardena, Thilina U. (Department of Marine Life Sciences, Jeju National University) ;
  • Sanjeewa, K.K. Asanka (Department of Marine Life Sciences, Jeju National University) ;
  • Kim, Hyun-Soo (National Marine Biodiversity Institute of Korea) ;
  • Lee, Hyo Geun (Department of Marine Life Sciences, Jeju National University) ;
  • Wang, Lei (Department of Marine Life Sciences, Jeju National University) ;
  • Lee, Dae-Sung (National Marine Biodiversity Institute of Korea) ;
  • Jeon, You-Jin (Department of Marine Life Sciences, Jeju National University)
  • Received : 2020.02.06
  • Accepted : 2020.02.28
  • Published : 2020.03.31
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Abstract

Background: The present study investigates the potent skin whitening ability of ethanol extract from the brown alga, Padina boryana (PBE) which was collected in the shores of Fulhadhoo Island, the Maldives, and its specific pathways of action. The effect of PBE which contains a rich amount of polyphenols was evaluated using B16F10 murine melanoma cells and provides insight to the underlying mechanisms with reference to the inhibition of melanin formation. Methods: Melanin synthesis and cellular tyrosinase inhibition were assessed in the α-MSH-stimulated melanocytes. Melanogenic pathway-related protein expressions were investigated via Western blotting. ERK 42/44 was particularly examined considering its involvement in the melanogenic pathway. Further, RT-qPCR techniques were involved in gene expression analysis. Results: PBE dose-dependently inhibited the cellular melanin synthesis and tyrosinase levels. Western blotting revealed the potential of PBE to downregulate microphthalmia-associated transcription factor (MITF), tyrosinase, and tyrosinase-related protein-1 and protein-2 (TRP-1 and TRP-2). Moreover, results explained the phosphorylation of ERK was sustained via PBE and hence declined the ultimate melanin synthesis. Gene expression analysis reinforced the results obtained. Conclusions: The study provides substantial evidence to express the potential of PBE to inhibit B16F10 melanoma cell melanin synthesis. Concisely, results suggest the ability of PBE to be involved in medicinal and cosmeceutical applications.

Keywords

References

  1. 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.
  2. Arung ET, Furuta S, Ishikawa H, Kusuma IW, Shimizu K, Kondo R. Antimelanogenesis properties of quercetin-and its derivative-rich extract from Allium cepa. Food chemistry. 2011;124:1024-8. https://doi.org/10.1016/j.foodchem.2010.07.067.
  3. Bae J-S, Han M, Yao C, Chung JH. Chaetocin inhibits IBMX-induced melanogenesis in B16F10 mouse melanoma cells through activation of ERK.Chemico-biological interactions. 2016;245:66-71. https://doi.org/10.1016/j.cbi.2015.12.021.
  4. Boonme P, Junyaprasert VB, Suksawad N, Songkro S. Microemulsions and nanoemulsions: novel vehicles for whitening cosmeceuticals. J Biomed Nanotechnol. 2009;5:373-83. https://doi.org/10.1166/jbn.2009.1046.
  5. Chan YY, Kim KH, Cheah SH. Inhibitory effects of Sargassum polycystum on tyrosinase activity and melanin formation in B16F10 murine melanoma cells. J Ethnopharmacol. 2011;137:1183-8. https://doi.org/10.1016/j.jep.2011.07.050.
  6. Chandler SF, Dodds JH. The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasodine in callus cultures of Solanum laciniatum. Plant Cell Rep. 1983;2:205-8. https://doi.org/10.1007/BF00270105.
  7. Heo SJ, Yoon WJ, Kim KN, Ahn GN, Kang SM, Kang DH, Affan A, Oh C, Jung WK, Jeon YJ. Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharide-stimulated RAW 264.7 macrophages. Food Chem Toxicol. 2010;48:2045-51. https://doi.org/10.1016/j.fct.2010.05.003.
  8. Herath K, Cho J, Kim A, Kim HS, Han EJ, Kim HJ, Kim MS, Ahn G, Jeon YJ, Jee Y. Differential modulation of immune response and cytokine profiles of Sargassum horneri ethanol extract in murine spleen with or without Concanavalin A stimulation. Biomed Pharmacother. 2019;110:930-42. https://doi.org/10.1016/j.biopha.2018.12.001.
  9. Huang H-C, Liao C-C, Peng C-C, Lim J-M, Siao J-H, Wei C-M, Chen C-C, Wu C-S, Chang T-M. Dihydromyricetin from Ampelopsis grossedentata inhibits melanogenesis through down-regulation of MAPK, PKA and PKC signaling pathways. Chem Biol Interact. 2016;258:166-74. https://doi.org/10.1016/j.cbi.2016.08.023.
  10. Ito S, Wakamatsu K. Quantitative analysis of eumelanin and pheomelanin in humans, mice, and other animals: a comparative review. Pigment Cell Res. 2003;16:523-31. https://doi.org/10.1034/j.1600-0749.2003.00072.x.
  11. Jayawardena TU, Asanka Sanjeewa KK, Shanura Fernando IP, Ryu BM, Kang MC, Jee Y, Lee WW, Jeon YJ. Sargassum horneri (Turner) C. Agardh ethanol extract inhibits the fine dust inflammation response via activating Nrf2/HO-1 signaling in RAW 264.7 cells. BMC Complement Altern Med. 2018;18:249. doi:https://doi.org/10.1186/s12906-018-2314-6.
  12. Jung HA, Hyun SK, Kim HR, Choi JS. Angiotensin-converting enzyme I inhibitory activity of phlorotannins from Ecklonia stolonifera. Fisheries Science. 2006;72:1292-9. https://doi.org/10.1111/j.1444-2906.2006.01288.x.
  13. 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;30:180-3. https://doi.org/10.1248/bpb.30.180.
  14. Kim DS, Kim SY, Chung JH, Kim KH, Eun HC, Park KC. Delayed ERK activation by ceramide reduces melanin synthesis in human melanocytes. Cell Signal. 2002;14:779-85. https://doi.org/10.1016/s0898-6568(02)00024-4.
  15. Kim H-S, Sanjeewa K, Fernando I, Ryu B, Yang H-W, Ahn G, Kang MC, Heo S-J, Je J-G, Jeon Y-J. A comparative study of Sargassum horneri Korea and China strains collected along the coast of Jeju Island South Korea: its components and bioactive properties. Algae. 2018;33:341-9. https://doi.org/10.4490/algae.2018.33.11.15.
  16. Kim KN, Yang HM, Kang SM, Kim D, Ahn G, Jeon YJ. Octaphlorethol A isolated from Ishige foliacea inhibits alpha-MSH-stimulated induced melanogenesis via ERK pathway in B16F10 melanoma cells. Food Chem Toxicol. 2013;59:521-6. https://doi.org/10.1016/j.fct.2013.06.031.
  17. Lee S. Anti-inflammatory mechanisms of phlorotannins derived from Eisenia bicyclis and their inhibitory effects on matrix metalloproteinases. Busan, South Korea: Pukyong National University; 2010.
  18. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-${\Delta}{\Delta}CT$ method. methods. 2001;25:402-408. doi:https://doi.org/10.1006/meth.2001.1262.
  19. Martinez-Esparza M, Jimenez-Cervantes C, Solano F, Lozano JA, Garcia-Borron JC. Mechanisms of melanogenesis inhibition by tumor necrosis factor-$\alpha$ in B16/F10 mouse melanoma cells. Eur J Biochem. 1998;255:139-46. https://doi.org/10.1046/j.1432-1327.1998.2550139.x.
  20. Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S, Lee YC. Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal Biochem. 2005;339:69-72. https://doi.org/10.1016/j.ab.2004.12.001.
  21. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55-63. https://doi.org/10.1016/0022-1759(83)90303-4.
  22. Nishimura T, Kometani T, Okada S, Ueno N, Yamamoto T. Inhibitory effects of hydroquinone-alpha-glucoside on melanin synthesis. Yakugaku Zasshi. 1995;115:626-32. https://doi.org/10.1248/yakushi1947.115.8_626.
  23. Ochanda SO, Faraj AK, Wanyoko JK, Onyango CA, Ruto HK. Extraction and quantification of total polyphenol content in different parts of selected tea cultivars. Am J Plant Sci. 2015;6:1581. https://doi.org/10.4236/ajps.2015.69158.
  24. Park HY, Kosmadaki M, Yaar M, Gilchrest BA. Cellular mechanisms regulating human melanogenesis. Cell Mol Life Sci. 2009;66:1493-506. https://doi.org/10.1007/s00018-009-8703-8.
  25. Park KT, Kim JK, Hwang D, Yoo Y, Lim YH. Inhibitory effect of mulberroside A and its derivatives on melanogenesis induced by ultraviolet B irradiation. Food Chem Toxicol. 2011;49:3038-45. https://doi.org/10.1016/j.fct.2011.09.008.
  26. Raper H. The aerobic oxidases. Physiological Reviews. 1928;8:245-82. https://doi.org/10.1152/physrev.1928.8.2.245.
  27. Sanjeewa KA, Park Y-j, Fernando IS, Ann Y-S, Ko C-I, Wang L, Jeon Y-J, Lee W. Soft corals collected from Jeju Island inhibits the $\alpha$-MSH-induced melanogenesis in B16F10 cells through activation of ERK. Fisheries and Aquatic Sciences. 2018;21:21. doi:https://doi.org/10.1186/s41240-018-0097-9.
  28. Sanjeewa KKA, Kim EA, Son KT, Jeon YJ. Bioactive properties and potentials cosmeceutical applications of phlorotannins isolated from brown seaweeds: a review. J Photochem Photobiol B. 2016;162:100-5. https://doi.org/10.1016/j.jphotobiol.2016.06.027.
  29. Sarangarajan R, Apte SP. The polymerization of melanin: a poorly understood phenomenon with egregious biological implications. Melanoma Res. 2006;16:3-10. https://doi.org/10.1097/01.cmr.0000195699.35143.df.
  30. Shibata T, Ishimaru K, Kawaguchi S, Yoshikawa H, Hama Y Antioxidant activities of phlorotannins isolated from Japanese Laminariaceae. In: Borowitzka MA, Critchley AT, Kraan S, Peters A, Sjotun K, Notoya M (eds) Nineteenth International Seaweed Symposium: Proceedings of the 19th International Seaweed Symposium, held in Kobe, Japan, 26-31 March, 2007. 2009;vol.Springer Netherlands, Dordrecht, pp 255-261. doi:https://doi.org/10.1007/978-1-4020-9619-8_32.
  31. Solano F, Briganti S, Picardo M, Ghanem G. Hypopigmenting agents: an updated review on biological, chemical and clinical aspects. Pigment Cell Res. 2006;19:550-71. https://doi.org/10.1111/j.1600-0749.2006.00334.x.
  32. Tomita Y, Maeda K, Tagami H. Melanocyte-stimulating properties of arachidonic acid metabolites: possible role in postinflammatory pigmentation. Pigment Cell Res. 1992;5:357-61. https://doi.org/10.1111/j.1600-0749.1992.tb00562.x.
  33. Vachtenheim J, Borovansky J. "Transcription physiology" of pigment formation in melanocytes: central role of MITF. Exp Dermatol. 2010;19:617-27. https://doi.org/10.1111/j.1600-0625.2009.01053.x.
  34. Vachtenheim J, Novotna H, Ghanem G. Transcriptional repression of the microphthalmia gene in melanoma cells correlates with the unresponsiveness of target genes to ectopic microphthalmia-associated transcription factor. J Invest Dermatol. 2001;117:1505-11. https://doi.org/10.1046/j.0022-202x.2001.01563.x.
  35. Wang L, Cui YR, Yang H-W, Lee HG, Ko J-Y, Jeon Y-J. A mixture of seaweed extracts and glycosaminoglycans from sea squirts inhibits $\alpha$-MSH-induced melanogenesis in B16F10 melanoma cells. Fisheries and Aquatic Sciences. 2019;22:11. https://doi.org/10.1186/s41240-019-0126-3.
  36. Wijesinghe WA, Jeon YJ. Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review. Fitoterapia. 2012;83:6-12. https://doi.org/10.1016/j.fitote.2011.10.016.
  37. Yao C, Oh J-h, Oh IG, Park C-h, Chung JH. [6]-Shogaol inhibits melanogenesis in B16 mouse melanoma cells through activation of the ERK pathway. Acta Pharmacol Sin 2013;34:289. doi:https://doi.org/10.1038/aps.2012.134.
  38. Yoon W, Kim M, Koh H, Lee W, Lee N, Hyun C. Effect of Korean red sea cucumber (Stichopus japonicus) on melanogenic protein expression in murine B16 melanoma. Int J Pharmacol. 2010;6:37-42. https://doi.org/10.3923/ijp.2010.37.42.

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