Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

The Inhibition of Melanogenesis Via the PKA and ERK Signaling Pathways by Chlamydomonas reinhardtii Extract in B16F10 Melanoma Cells and Artificial Human Skin Equivalents

  • Lee, Ayeong (Research Institute for Molecular-Targeted Drugs, Department of Cosmetics Engineering, Konkuk University) ;
  • Kim, Ji Yea (Research Institute for Molecular-Targeted Drugs, Department of Cosmetics Engineering, Konkuk University) ;
  • Heo, Jina (Sustainable Bioresource Research Center, KRIBB) ;
  • Cho, Dae-Hyun (Sustainable Bioresource Research Center, KRIBB) ;
  • Kim, Hee-Sik (Sustainable Bioresource Research Center, KRIBB) ;
  • An, In-Sook (Korea Institute for Skin and Clinical Sciences, Gene Cell Pharm Corporation) ;
  • An, Sungkwan (Research Institute for Molecular-Targeted Drugs, Department of Cosmetics Engineering, Konkuk University) ;
  • Bae, Seunghee (Research Institute for Molecular-Targeted Drugs, Department of Cosmetics Engineering, Konkuk University)
  • Received : 2018.10.04
  • Accepted : 2018.10.29
  • Published : 2018.12.28
Download PDF
⟨ Previous Next ⟩

Abstract

Abnormal melanin synthesis results in several hyperpigmentary disorders such as freckles, melanoderma, age spots, and other related conditions. In this study, we investigated the anti-melanogenic effects of an extract from the microalgae Chlamydomonas reinhardtii (CE) and potential mechanisms responsible for its inhibitory effect in B16F10, normal human epidermal melanocyte cells, and human skin-equivalent models. The CE extract showed significant dose-dependent inhibitory effects on ${\alpha}$-melanocyte-stimulating, hormone-induced melanin synthesis in cells. Additionally, the CE extract exhibited suppressive effects on the mRNA and protein expression of microphthalmia-associated transcription factor, tyrosinase, tyrosinase-related protein-1, and tyrosinase-related protein-2. The CE extract also inhibited the phosphorylation of protein kinase A and extracellular signal-related kinase, which function as upstream regulators of melanogenesis. Using a three-dimensional, reconstructed pigmented epidermis model, the CE-mediated, anti-pigmentation effects were confirmed by Fontana-Masson staining and melanin content assays. Taken together, CE extract can be used as an anti-pigmentation agent.

Keywords

References

  1. Wasmeier C, Hume AN, Bolasco G, Seabra MC. 2008. Melanosomes at a glance. J. Cell Sci. 121: 3995-3999. https://doi.org/10.1242/jcs.040667
  2. Slominski A, Tobin DJ, Shibahara S, Wortsman J. 2004. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 84: 1155-1228. https://doi.org/10.1152/physrev.00044.2003
  3. Kadekaro AL, Chen J, Yang J, Chen S, Jameson J, Swope VB, et al. 2012. Alpha-melanocyte-stimulating hormone suppresses oxidative stress through a p53-mediated signaling pathway in human melanocytes. Mol. Cancer Res. 10: 778-786. https://doi.org/10.1158/1541-7786.MCR-11-0436
  4. Passeron T, Mantoux F, Ortonne JP. 2005. Genetic d isorders of pigmentation. Clin. Dermatol. 23: 56-67. https://doi.org/10.1016/j.clindermatol.2004.09.013
  5. Schallreuter KU, Kothari S, Chavan B, Spencer JD. 2008. Regulation of melanogenesis--controversies and new concepts. Exp. Dermatol. 17: 395-404. https://doi.org/10.1111/j.1600-0625.2007.00675.x
  6. Naish-Byfield S, Riley PA. 1998. Tyrosinase kinetics: failure of acceleration in oxidation of ring-blocked monohydric phenol substrate. Pigment Cell Res. 11: 94-97. https://doi.org/10.1111/j.1600-0749.1998.tb00716.x
  7. Chan C-F, Huang C-C, Lee M-Y, Lin Y-S. 2014. Fermented broth in tyrosinase- and melanogenesis inhibition. Molecules 19: 13122-13135. https://doi.org/10.3390/molecules190913122
  8. Bentley NJ, Eisen T, Goding CR. 1994. Melanocyte-specific expression of the human tyrosinase promoter: activation by the microphthalmia gene product and role of the initiator. Mol. Cell. Biol. 14: 7996-8006. https://doi.org/10.1128/MCB.14.12.7996
  9. Bonaventure J, Domingues MJ, Larue L. 2013. Cellular and molecular mechanisms controlling the migration of melanocytes and melanoma cells. Pigment Cell Melanoma Res. 26: 316-325. https://doi.org/10.1111/pcmr.12080
  10. Shibahara S, Yasumoto K, Amae S, Udono T, Watanabe K, Saito H, et al. 2000. Regulation of pigment cell-specific gene expression by MITF. Pigment Cell Res. 13 (Suppl) 8: 98-102. https://doi.org/10.1034/j.1600-0749.13.s8.18.x
  11. Wang HM, Chen CC, Huynh P, Chang JS. 2015. Exploring the potential of using algae in cosmetics. Bioresour. Technol. 184: 355-362. https://doi.org/10.1016/j.biortech.2014.12.001
  12. Zhao X, Xue C-H, Li Z-J, Cai Y-P, Liu H-Y, Qi H-T. 2004. Antioxidant and hepatoprotective activities of low molecular weight sulfated polysaccharide from Laminaria japonica. J. Appl. Phycol. 16: 111-115. https://doi.org/10.1023/B:JAPH.0000044822.10744.59
  13. Kosourov S, Tsygankov A, Seibert M, Ghirardi ML. 2002. Sustained hydrogen photoproduction by Chlamydomonas reinhardtii: effects of culture parameters. Biotechnol. Bioeng. 78: 731-740. https://doi.org/10.1002/bit.10254
  14. Guedes AC, Amaro HM, M alcata FX. 2011. Microalgae as sources of carotenoids. Marine Drugs 9: 625-644. https://doi.org/10.3390/md9040625
  15. Lee JJ, An S, Kim KB, Heo J, Cho DH, Oh HM, et al. 2016. Extract of Ettlia sp. YC001 exerts photoprotective effects against UVB irradiation in normal human dermal fibroblasts. J. Microbiol. Biotechnol. 26: 775-783. https://doi.org/10.4014/jmb.1509.09067
  16. Heo J, Shin D-S, Cho K, Cho D-H, Lee YJ, Kim H-S. 2018. Indigenous microalga Parachlorella sp. JD-076 as a potential source for lutein production: optimization of lutein productivity via regulation of light intensity and carbon source. Algal Res. 33: 1-7. https://doi.org/10.1016/j.algal.2018.04.029
  17. D'Mello S, Finlay G, Baguley B, Askarian-Amiri M. 2016. Signaling pathways in melanogenesis. Int. J. Mol. Sci. 17: E1144. https://doi.org/10.3390/ijms17071144
  18. Shimoda H, Tanaka J, Shan SJ, Maoka T. 2010. Antipigmentary activity of fucoxanthin and its influence on skin mRNA expression of melanogenic molecules. J. Pharm. Pharmacol. 62: 1137-1145. https://doi.org/10.1111/j.2042-7158.2010.01139.x
  19. Camera E, Mastrofrancesco A, Fabbri C, Daubrawa F, Picardo M, Sies H, et al. 2009. Astaxanthin, canthaxanthin and beta-carotene differently affect UVA-induced oxidative damage and expression of oxidative stress-responsive enzymes. Exp. Dermatol. 18: 222-231. https://doi.org/10.1111/j.1600-0625.2008.00790.x
  20. Ichihashi M, Ueda M, Budiyanto A, Bito T, Oka M, Fukunaga M, et al. 2003. UV-induced skin damage. Toxicology 189: 21-39. https://doi.org/10.1016/S0300-483X(03)00150-1
  21. Fiedor J, Burda K. 2014. Potential role of carotenoids as antioxidants in human health and disease. Nutrients 6: 466-488. https://doi.org/10.3390/nu6020466
  22. Dai J, Mumper RJ. 2010. Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15: 7313-7352. https://doi.org/10.3390/molecules15107313
  23. Rasouli H, Farzaei MH, Khodarahmi R. 2017. Polyphenols and their benefits: a review. Int. J. Food Prop. 20: 1700-1741. https://doi.org/10.1080/10942912.2016.1193515
  24. Chang T-S. 2009. An updated review of tyrosinase inhibitors. Int. J. Mol. Sci. 10: 2440-2475. https://doi.org/10.3390/ijms10062440
  25. Baek Sh, Lee SH. 2015. Sesamol decreases melanin biosynthesis in melanocyte cells and zebrafish: Possible involvement of MITF via the intracellular cAMP and p38/JNK signalling pathways. Exp. Dermatol. 24: 761-766. https://doi.org/10.1111/exd.12765
  26. Hartman ML, Czyz M. 2015. MITF in melanoma: mechanisms behind its expression and activity. Cell. Mol. Life Sci. 72: 1249-1260. https://doi.org/10.1007/s00018-014-1791-0
  27. Burger P, Landreau A, Azoulay S, Michel T, Fernandez X. 2016. Skin whitening cosmetics: feedback and challenges in the development of natural skin lighteners. Cosmetics 3: 36. https://doi.org/10.3390/cosmetics3040036
  28. Bae-Harboe YS, Park HY. 2012. Tyrosinase: a central regulatory protein for cutaneous pigmentation. J. Invest. Dermatol. 132: 2678-2680. https://doi.org/10.1038/jid.2012.324
  29. Roh E, Yun C-Y, Yun JY, Park D, Kim ND, Hwang BY, et al. 2013. cAMP-binding site of PKA as a molecular target of bisabolangelone against melanocyte-specific hyperpigmented disorder. J. Invest. Dermatol. 133: 1072-1079. https://doi.org/10.1038/jid.2012.425
  30. Yun C-Y, Ko SM, Choi YP, Kim BJ, Lee J, Kim JM, et al. 2018. ${\alpha}$-Viniferin improves facial hyperpigmentation via accelerating feedback termination of cAMP/PKA-signaled phosphorylation circuit in facultative melanogenesis. Theranostics 8: 2031-2043. https://doi.org/10.7150/thno.24385
  31. Jiang Z, Li S, Liu Y, Deng P, Huang J, He G. 2011. Sesamin induces melanogenesis by microphthalmia-associated transcription factor and tyrosinase up-regulation via cAMP signaling pathway. Acta Biochim. Biophys. Sin. 43: 763-770. https://doi.org/10.1093/abbs/gmr078
  32. Hemesath TJ, Price ER, Takemoto C, Badalian T, Fisher DE. 1998. MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature 391: 298-301. https://doi.org/10.1038/34681
  33. Imokawa G, Yada Y, Kimura M. 1996. Signalling mechanisms of endothelin-induced mitogenesis and melanogenesis in human melanocytes. Biochem. J. 314 (Pt 1): 305-312. https://doi.org/10.1042/bj3140305
  34. Ye Y, Wang H, Chu JH, Chou GX, Yu ZL. 2011. Activation of p38 MAPK pathway contributes to the melanogenic property of apigenin in B16 cells. Exp. Dermatol. 20: 755-757. https://doi.org/10.1111/j.1600-0625.2011.01297.x
  35. Saha B, Singh SK, Sarkar C, Bera R, Ratha J, Tobin DJ, et al. 2006. Activation of the Mitf promoter by lipid-stimulated activation of p38-stress signalling to CREB. Pigment Cell Res. 19: 595-605. https://doi.org/10.1111/j.1600-0749.2006.00348.x
  36. Yanase H, Ando H, Horikawa M, Watanabe M, Mori T, Matsuda N. 2001. Possible involvement of ERK 1/2 in UVAinduced melanogenesis in cultured normal human epidermal melanocytes. Pigment Cell Res. 14: 103-109. https://doi.org/10.1034/j.1600-0749.2001.140205.x
  37. Englaro W, Rezzonico R, Durand-Clement M, Lallemand D, Ortonne JP, Ballotti R. 1995. Mitogen-activated protein kinase pathway and AP-1 are activated during cAMP-induced melanogenesis in B-16 melanoma cells. J. Biol. Chem. 270: 24315-24320. https://doi.org/10.1074/jbc.270.41.24315
  38. Kim DS, Hwang ES, Lee JE, Kim SY, Kwon SB, Park KC. 2003. Sphingosine-1-phosphate decreases melanin synthesis via sustained ERK activation and subsequent MITF degradation. J. Cell Sci. 116: 1699-1706. https://doi.org/10.1242/jcs.00366
  39. Yoon TJ, Lei TC, Yamaguchi Y, Batzer J, Wolber R, Hearing VJ. 2003. Reconstituted 3-dimensional human skin of various ethnic origins as an in vitro model for studies of pigmentation. Anal. Biochem. 318: 260-269. https://doi.org/10.1016/S0003-2697(03)00172-6
  40. Kandarova H, Liebsch M, Spielmann H, Genschow E, Schmidt E, Traue D, et al. 2006. Assessment of the human epidermis model SkinEthic RHE for in vitro skin corrosion testing of chemicals according to new OECD TG 431. Toxicol. In Vitro 20: 547-559. https://doi.org/10.1016/j.tiv.2005.11.008
  41. Kidd DA, Johnson M, Clements J. 2007. Development of an in vitro corrosion/irritation prediction assay using the EpiDerm skin model. Toxicol. In Vitro 21: 1292-1297. https://doi.org/10.1016/j.tiv.2007.08.018

Cited by

  1. Loganin Inhibits α-MSH and IBMX-induced Melanogenesis by Suppressing the Expression of Tyrosinase in B16F10 Melanoma Cells vol.29, pp.11, 2019, https://doi.org/10.5352/jls.2019.29.11.1200
  2. Photoprotection and Skin Pigmentation: Melanin-Related Molecules and Some Other New Agents Obtained from Natural Sources vol.25, pp.7, 2018, https://doi.org/10.3390/molecules25071537
  3. Jeju Magma-Seawater Inhibits α-MSH-Induced Melanogenesis via CaMKKβ-AMPK Signaling Pathways in B16F10 Melanoma Cells vol.18, pp.9, 2018, https://doi.org/10.3390/md18090473
  4. Antimelanogenesis Effects of Theasinensin A vol.22, pp.14, 2018, https://doi.org/10.3390/ijms22147453
  5. Evaluation of Anti-Melanogenesis Activity of Enriched Pueraria lobata Stem Extracts and Characterization of Its Phytochemical Components Using HPLC-PDA-ESI-MS/MS vol.22, pp.15, 2018, https://doi.org/10.3390/ijms22158105