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Chemical Composition and Tyrosinase Inhibitory Activities of Fatty Acids Obtained from Heterotrophic Microalgae, S. limacinum and C. cohnii

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Abstract

Tyrosinase is the rate-limiting enzyme for melanin production in plant and mammalian cells. Upregulation of this enzyme results in hyperpigmentation disorders. In order to treat pigmentation problems, novel skin whitening compounds are extremely screened. It is found that fatty acids based on their saturation levels either increase or decrease tyrosinase enzyme activity. Thus, fatty acids and their compositions are promising candidates for the treatment of hyperpigmentation or hypopigmentation disorders. Microalgae are rich in both saturated and unsaturated fatty acids, as well. In this study, C. cohnii and S. limacinum fatty acids were evaluated as tyrosinase inhibitor candidates. Mushroom tyrosinase activity studies displayed that both extracts increase tyrosinase enzyme activity dose-dependently. On the other hand, S. limacinum at 200 µg ml−1 concentration almost decreased half of tyrosinase enzyme activity in B16-F10 cells. Besides, it was 3 times more efficient for tyrosinase enzyme activity inhibition and 2 times more effective to decrease melanin synthesis compared to C. cohnii. Considering low toxicity to B16-F10 melanoma and healthy keratinocyte cells (HaCaT), S. limacinum fatty acids could be a suitable source for lipid-based tyrosinase inhibitory functional cosmetics products.

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References

  1. Chang, T. S. (2012). Natural melanogenesis inhibitors acting through the down-regulation of tyrosinase activity. Materials, 5(9), 1661–1685. https://doi.org/10.3390/ma5091661

    Article  CAS  Google Scholar 

  2. D’Mello, S. A. N., Finlay, G. J., Baguley, B. C., & Askarian-Amiri, M. E. (2016). Signaling pathways in melanogenesis. International Journal of Molecular Sciences, 17(7), 1–18. https://doi.org/10.3390/ijms17071144

    Article  CAS  Google Scholar 

  3. Heo, S. J., Ko, S. C., Cha, S. H., Kang, D. H., Park, H. S., Choi, Y. U., & Jeon, Y. J. (2009). Effect of phlorotannins isolated from Ecklonia cava on melanogenesis and their protective effect against photo-oxidative stress induced by UV-B radiation. Toxicology in Vitro. https://doi.org/10.1016/j.tiv.2009.05.013

    Article  Google Scholar 

  4. Pillaiyar, T., Namasivayam, V., Manickam, M., & Jung, S. H. (2018). Inhibitors of melanogenesis: An updated review. Journal of Medicinal Chemistry, 61(17), 7395–7418. https://doi.org/10.1021/acs.jmedchem.7b00967

    Article  CAS  Google Scholar 

  5. Oh, T. I., Yun, J. M., Park, E. J., Kim, Y. S., Lee, Y. M., & Lim, J. H. (2017). Plumbagin suppresses α-MSH-induced melanogenesis in B16F10 mouse melanoma cells by inhibiting tyrosinase activity. International Journal of Molecular Sciences, 18(2). https://doi.org/10.3390/ijms18020320

  6. Chan, C. F., Huang, C. C., Lee, M. Y., & Lin, Y. S. (2014). Fermented broth in tyrosinase- and melanogenesis inhibition. Molecules, 19(9), 13122–13135. https://doi.org/10.3390/molecules190913122

    Article  CAS  Google Scholar 

  7. Kubglomsong, S., Theerakulkait, C., Reed, R. L., Yang, L., Maier, C. S., & Stevens, J. F. (2018). Isolation and identification of tyrosinase-inhibitory and copper-chelating peptides from hydrolyzed rice-bran-derived albumin. Journal of Agricultural and Food Chemistry, 66(31), 8346–8354. research-article. https://doi.org/10.1021/acs.jafc.8b01849

  8. Wang, Z. J., Si, Y. X., Oh, S., Yang, J. M., Yin, S. J., Park, Y. D., & Qian, G. Y. (2012). The effect of fucoidan on tyrosinase: Computational molecular dynamics integrating inhibition kinetics. Journal of Biomolecular Structure and Dynamics, 30(4), 460–473. https://doi.org/10.1080/07391102.2012.682211

    Article  CAS  Google Scholar 

  9. Ephrem, E., Elaissari, H., & Greige-Gerges, H. (2017). Improvement of skin whitening agents efficiency through encapsulation: Current state of knowledge. International Journal of Pharmaceutics, 526(1–2), 50–68. https://doi.org/10.1016/j.ijpharm.2017.04.020

    Article  CAS  Google Scholar 

  10. Kose, A., & Oncel, S. S. (2015). Properties of microalgal enzymatic protein hydrolysates: Biochemical composition, protein distribution and FTIR characteristics. Biotechnology Reports, 6, 137–143. https://doi.org/10.1016/J.BTRE.2015.02.005

    Article  CAS  Google Scholar 

  11. Garc ıa, J. L., de Vicente, M., & Gal an, B. (n.d.). Microalgae, old sustainable food and fashion nutraceuticals. https://doi.org/10.1111/1751-7915.12800

  12. Nishigaki, I., Peramaiyan, R., Ramachandran, V., Gnapathy, E., Dhanapal, S., & Yutaka, N. (2010). Cytoprotective role of astaxanthin against glycated protein/iron chelate-induced toxicity in human umbilical vein endothelial cells. Phytotherapy Research, 24(June), 54–59. https://doi.org/10.1002/ptr

    Article  CAS  Google Scholar 

  13. Jain, S., Prajapat, G., Abrar, M., Ledwani, L., Singh, A., & Agrawal, A. (2017). Cyanobacteria as efficient producers of mycosporine-like amino acids. Journal of Basic Microbiology. https://doi.org/10.1002/jobm.201700044

    Article  Google Scholar 

  14. Pratoomthai, B., Songtavisin, T., Gangnonngiw, W., & Wongprasert, K. (n.d.). In vitro inhibitory effect of sulfated galactans isolated from red alga Gracilaria fisheri on melanogenesis in B16F10 melanoma cells. https://doi.org/10.1007/s10811-018-1469-3

  15. Rao, A. R., Sindhuja, H. N., Dharmesh, S. M., Sankar, K. U., Sarada, R., & Ravishankar, G. A. (2013). Effective inhibition of skin cancer, tyrosinase, and antioxidative properties by astaxanthin and astaxanthin esters from the green alga haematococcus pluvialis. Journal of Agricultural and Food Chemistry, 61(16), 3842–3851. https://doi.org/10.1021/jf304609j

    Article  CAS  Google Scholar 

  16. Custódio, L., Soares, F., Pereira, H., Rodrigues, M. J., Barreira, L., Rauter, A. P., & Varela, J. (2015). Botryococcus braunii and Nannochloropsis oculata extracts inhibit cholinesterases and protect human dopaminergic SH-SY5Y cells from H2O2-induced cytotoxicity. Journal of Applied Phycology, 27(2), 839–848. https://doi.org/10.1007/s10811-014-0369-4

    Article  CAS  Google Scholar 

  17. Levy-Ontman, O., Huleihel, M., Hamias, R., Wolak, T., & Paran, E. (2017). An anti-inflammatory effect of red microalga polysaccharides in coronary artery endothelial cells. Atherosclerosis, 264, 11–18. https://doi.org/10.1016/j.atherosclerosis.2017.07.017

    Article  CAS  Google Scholar 

  18. Isleten-Hosoglu, M., & Elibol, M. (2017). Improvement of medium composition and cultivation conditions for growth and lipid production by Crypthecodinium cohnii. Romanian Biotechnological Letters, 22(6), 13086–13095.

    CAS  Google Scholar 

  19. Sahin, D., Tas, E., & Altindag, U. H. (2018). Enhancement of docosahexaenoic acid (DHA) production from Schizochytrium sp. S31 using different growth medium conditions. AMB Express, 8(1). https://doi.org/10.1186/s13568-018-0540-4

  20. Ando, H., Watabe, H., Valencia, J. C., Yasumoto, K., Furumura, M., Funasaka, Y., & Hearing, V. J. (2004). Fatty acids regulate pigmentation via proteasomal degradation of tyrosinase. Journal of Biological Chemistry, 279(15), 15427–15433. https://doi.org/10.1074/jbc.m313701200

    Article  CAS  Google Scholar 

  21. Balcos, M. C., Kim, S. Y., Jeong, H., Yun, H., Baek, K. J., Kwon, N. S., & Kim, D. (2014). Docosahexaenoic acid inhibits melanin synthesis in murine melanoma cells in vitro through increasing tyrosinase degradation. Nature Publishing Group, 1, 489–495. https://doi.org/10.1038/aps.2013.174

    Article  CAS  Google Scholar 

  22. Cui, H. X., Duan, F. F., Jia, S. S., Cheng, F. R., & Yuan, K. (2018). Antioxidant and tyrosinase inhibitory activities of seed oils from Torreya grandis Fort. ex Lindl. BioMed Research International, 2018. https://doi.org/10.1155/2018/5314320

  23. Yildiztekin, F., Nadeem, S., Erol, E., Yildiztekin, M., Tuna, A. L., & Ozturk, M. (2016). Antioxidant, anticholinesterase and tyrosinase inhibition activities, and fatty acids of Crocus mathewii – A forgotten endemic angiosperm of Turkey. Pharmaceutical Biology, 54(9), 1557–1563. https://doi.org/10.3109/13880209.2015.1107746

    Article  CAS  Google Scholar 

  24. Isleten-Hosoglu, M., Gultepe, I., & Elibol, M. (2012). Optimization of carbon and nitrogen sources for biomass and lipid production by Chlorella saccharophila under heterotrophic conditions and development of Nile red fluorescence based method for quantification of its neutral lipid content. Biochemical Engineering Journal, 61, 11–19. https://doi.org/10.1016/J.BEJ.2011.12.001

    Article  CAS  Google Scholar 

  25. Chan, Y. Y., Kim, K. H., & Cheah, S. H. (2011). Inhibitory effects of Sargassum polycystum on tyrosinase activity and melanin formation in B16F10 murine melanoma cells. Journal of Ethnopharmacology. https://doi.org/10.1016/j.jep.2011.07.050

    Article  Google Scholar 

  26. Sun, L., Guo, Y., Zhang, Y., & Zhuang, Y. (2017). Antioxidant and anti-tyrosinase activities of phenolic extracts from rape bee pollen and inhibitory melanogenesis by cAMP/MITF/TYR pathway in B16 mouse melanoma cells. Frontiers in Pharmacology, 8(MAR), 1–9. https://doi.org/10.3389/fphar.2017.00104

  27. Fistarol, S. K., & Itin, P. H. (2010). Disorders of pigmentation, 2010(Band 8), 187–202. https://doi.org/10.1111/j.1610-0387.2009.07137.x

  28. Chang, T. S. (2009). An updated review of tyrosinase inhibitors. International Journal of Molecular Sciences, 10(6), 2440–2475. https://doi.org/10.3390/ijms10062440

    Article  CAS  Google Scholar 

  29. Wang, L. X., Qian, J., Zhao, L. N., & Zhao, S. H. (2018). Effects of volatile oil from ginger on the murine B16 melanoma cells and its mechanism. Food and Function, 9(2), 1058–1069. https://doi.org/10.1039/c7fo01127j

    Article  CAS  Google Scholar 

  30. Tel, G., Öztürk, M., Duru, M. E., Doǧan, B., & Harmandar, M. (2013). Fatty acid composition, antioxidant, anticholinesterase and tyrosinase inhibitory activities of four Serratula species from anatolia. Records of Natural Products, 7(2), 86–95.

    CAS  Google Scholar 

  31. Shabani, F., & Sariri, R. (2010). Increase of melanogenesis in the presence of fatty acids. Pharmacologyonline, 1, 314–323.

    Google Scholar 

  32. Jeon, S., Kim, N. H., Koo, B. S., Kim, J. Y., & Lee, A. Y. (2009). Lotus (Nelumbo nuficera) flower essential oil increased melanogenesis in normal human melanocytes. Experimental and Molecular Medicine, 41(7), 517–524. https://doi.org/10.3858/emm.2009.41.7.057

    Article  CAS  Google Scholar 

  33. Chaikul, P., Sripisut, T., Chanpirom, S., Sathirachawan, K., & Ditthawuthikul, N. (2017). Melanogenesis inhibitory and antioxidant effects of Camellia oleifera seed oil. Advanced Pharmaceutical Bulletin, 7(3), 473–477. https://doi.org/10.15171/apb.2017.057

  34. Matsuura, R., Ukeda, H., & Sawamura, M. (2006). Tyrosinase inhibitory activity of citrus essential oils. Journal of Agricultural and Food Chemistry, 54(6), 2309–2313. https://doi.org/10.1021/jf051682i

    Article  CAS  Google Scholar 

  35. Zajdel, A., Wilczok, A., Chodurek, E., Gruchlik, A., & Dzierzewicz, Z. (2013). Polyunsaturated fatty acids inhibit melanoma cell growth in vitro. Acta Poloniae Pharmaceutica - Drug Research, 70(2), 365–369.

    CAS  Google Scholar 

  36. Tan, R., Wang, F., Fan, C., & Zhang, X. (2018). Function suppresses B16F10 melanoma lung metastasis by autophagy induction. 6179–6186. https://doi.org/10.1039/c8fo01617h

  37. Mericli, F., Becer, E., Kabadayi, H., Hanoglu, A., Hanoglu, D. Y., Yavuz, D. O., & Vatansever, S. (2017). Fatty acid composition and anticancer activity in colon carcinoma cell lines of Prunus dulcis seed oil. Pharmaceutical Biology, 55(1), 1239–1248. https://doi.org/10.1080/13880209.2017.1296003

    Article  CAS  Google Scholar 

  38. Schauss, A. G. (2016). Advances in the study of the health benefits and mechanisms of action of the pulp and seed of the Amazonian palm fruit, Euterpe oleracea Mart., known as “Açai.” Fruits, Vegetables, and Herbs: Bioactive Foods in Health Promotion, 48, 179–220. https://doi.org/10.1016/B978-0-12-802972-5.00010-X

    Article  Google Scholar 

  39. Santos, A., Andres, E., Medina, S. P. H., Ferrari, C. R., & Lourenc, C. B. (2012). Schinus terebinthifolius Raddi extract and linoleic acid from Passiflora edulis synergistically decrease melanin synthesis in B16 cells and reconstituted epidermis. 435–440. https://doi.org/10.1111/j.1468-2494.2012.00736.x

  40. Kose, A., & Oncel, S. S. (2017). Algae as a promising resource for biofuel industry: Facts and challenges. International Journal of Energy Research, 41(7), 924–951. https://doi.org/10.1002/er.3699

    Article  Google Scholar 

  41. Borowitzka, M. A. (2013). High-value products from microalgae-their development and commercialisation. Journal of Applied Phycology, 25(3), 743–756. https://doi.org/10.1007/s10811-013-9983-9

    Article  CAS  Google Scholar 

  42. Shigeta, Y., Imanaka, H., Ando, H., Ryu, A., Oku, N., Baba, N., & Makino, T. (2004). Skin whitening effect of linoleic acid is enhanced by liposomal formulations. Biological and Pharmaceutical Bulletin, 27(4), 591–594. https://doi.org/10.1248/bpb.27.591

    Article  CAS  Google Scholar 

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Acknowledgements

This research study was done at Ege University Bioengineering Department, Microalgal Bioprocess lab. The author would like to thank Assoc. Prof. Dr. Suphi S. Oncel and Prof. Dr. Murat Elibol for their valuable contribution.

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  1. Department of Bioengineering, Faculty of Engineering, University of Ege, 35100, Bornova, Izmir, Turkey

    Ayse Kose

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Ayse Kose (AK) designed the experiments, conducted the analysis, and wrote the manuscript.

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Correspondence to Ayse Kose.

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Kose, A. Chemical Composition and Tyrosinase Inhibitory Activities of Fatty Acids Obtained from Heterotrophic Microalgae, S. limacinum and C. cohnii. Appl Biochem Biotechnol 195, 369–385 (2023). https://doi.org/10.1007/s12010-022-04143-9

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