Browse > Article
http://dx.doi.org/10.14348/molcells.2015.2263

Lipoteichoic Acid Isolated from Lactobacillus plantarum Inhibits Melanogenesis in B16F10 Mouse Melanoma Cells  

Kim, Hye Rim (School of Biotechnology and Institute of Life Science and Resources, College of Life Science, Kyung Hee University)
Kim, Hangeun (School of Biotechnology and Institute of Life Science and Resources, College of Life Science, Kyung Hee University)
Jung, Bong Jun (School of Biotechnology and Institute of Life Science and Resources, College of Life Science, Kyung Hee University)
You, Ga Eun (School of Biotechnology and Institute of Life Science and Resources, College of Life Science, Kyung Hee University)
Jang, Soojin (Institute Pasteur Korea)
Chung, Dae Kyun (School of Biotechnology and Institute of Life Science and Resources, College of Life Science, Kyung Hee University)
Abstract
Lipoteichoic acid (LTA) is a major component of the cell wall of Gram-positive bacteria. Its effects on living organisms are different from those of lipopolysaccharide (LPS) found in Gram-negative bacteria. LTA contributes to immune regulatory effects including anti-aging. In this study, we showed that LTA isolated from Lactobacillus plantarum (pLTA) inhibited melanogenesis in B16F10 mouse melanoma cells. pLTA reduced the cellular activity of tyrosinase and the expression of tyrosinase family members in a dose-dependent manner. The expression of microphthalmia- associated transcription factor (MITF), a key factor in the synthesis of melanin, was also decreased by pLTA. Further, we showed that pLTA activated melanogenesis signaling, such as extracellular signal-regulated kinase (ERK) and phosphatidylinositol 3-kinse (PI3K)/AKT. In addition, the expression of heterogeneous nuclear ribonucleoprotein A1 (hnRNP A1) and HuR, which are important RNA-binding proteins (RBPs), was reduced. pLTA likely degrades MITF via regulation of melanogenic signaling and RNA stability of melanogenic proteins, resulting in the reduction of melanin. Thus, our data suggest that pLTA has therapeutic potential for treating hyperpigmentation disorders and can also be used as a cosmetic whitening agent.
Keywords
Lactobacillus plantarum; lipoteichoic acid; melanogenesis; microphthalmia-associated transcription factor (MITF); RNA stability;
Citations & Related Records
Times Cited By KSCI : 3  (Citation Analysis)
연도 인용수 순위
1 Kim, H.G., Kim, N.R., Gim, M.G., Lee, J.M., Lee, S.Y., Ko, M.Y., Kim, J.Y., Han, S.H., and Chung, D.K. (2008a). Lipoteichoic acid isolated from Lactobacillus plantarum inhibits lipopolysaccharideinduced $TNF-{\alpha}$ production in THP-1 cells and endotoxin shock in mice. J. Immunol. 180, 2553-2561.   DOI
2 Kim, H.G., Lee, S.Y., Kim, N.R., Ko, M.Y., Lee, J.M., Yi, T.H,, Chung, S.K., and Chung, D.K. (2008b). Inhibitory Effects of Lactobacillus plantarum Lipoteichoic Acid (LTA) on Staphylococcus aureus LTA-Induced Tumor Necrosis Factor-Alpha Production. J. Microbiol. Biotechnol. 18, 1191-1196.
3 Kim, S., Jung, S.H., and Cho, C.W. (2008c). Physicochemical studies of a newly synthesized molecule, 6-methyl-3-phenethyl-3,4- dihydro-1H-quinazoline-2-thione (JSH18) for topical formulations. Arch. Pharm. Res. 31, 1363-1368.   DOI   ScienceOn
4 Koo, J.H., Lee, I., Yun, S.K., Kim, H.U., Park, B.H., and Park, J.W. (2010). Saponified evening primrose oil reduces melanogenesis in B16 melanoma cells and reduces UV-induced skin pigmentation in humans. Lipids 45, 401-407.   DOI   ScienceOn
5 Lee, J., Jung, K., Kim, Y.S., and Park, D. (2007). Diosgenin inhibits melanogenesis through the activation of phosphatidylinositol-3- kinase pathway (PI3K) signaling. Life Sci. 81, 249-254.   DOI   ScienceOn
6 Lee, J.E., Kim, S.Y., Jeong, Y.M., Yun, H.Y., Baek, K.J., Kwon, N.S., Park, K.C., and Kim, D.S. (2010). The regulatory mechanism of melanogenesis by FTY720, a sphingolipid analogue. Exp. Dermatol. 20, 237-241.
7 Li, G., Ju, H.K., Chang, H.W., Jahng, Y., Lee, S.H., and Son, J.K. (2003). Melanin biosynthesis inhibitors from the bark of Machilus thunbergii. Biol. Pharm. Bull. 26, 1039-1041.   DOI   ScienceOn
8 Lin, J.Y., and Fisher, D.E. (2007). Melanocyte biology and skin pigmentation. Nature 445, 843-850.   DOI   ScienceOn
9 Meinkoth, J.L., Montminy, M.R., Fink, J.S., and Feramisco, J.R. (1991). Induction of a cyclic AMP-responsive gene in living cells requires the nuclear factor CREB. Mol. Cell. Biol. 11, 1759-1764.   DOI
10 Morrison, D.C., Ryan, J.L. (1987). Endotoxins and disease mechanisms. Annu. Rev. Med. 38, 417-432.   DOI   ScienceOn
11 Papadopoulou, C., Patrinou-Georgoula, M., and Guialis, A. (2010). Extensive association of HuR with hnRNP proteins within immunoselected hnRNP and mRNP complexes. Biochim. Biophys. Acta 1804, 692-703.   DOI   ScienceOn
12 Papadopoulou, C., Ganou, V., Patrinou-Georgoula, M., and Guialis, A. (2013). HuR-hnRNP interactions and the effect of cellular stress. Mol. Cell 372, 137-147.
13 Park, S.Y., Jin, M.L., Kim, Y.H., Kim, Y., and Lee, S.J. (2011). Aromatic- turmerone inhibits ${\alpha}-MSH$ and IBMX-induced melanogenesis by inactivating CREB and MITF signaling pathways. Arch. Dermatol. Res. 303, 737-744.   DOI
14 Parvez, S., Malik, K.A., Ah Kang, S., and Kim, H.Y. (2006). Probiotics and their fermented food products are beneficial for health. J. Appl. Microbiol. 100, 1171-1185.   DOI   ScienceOn
15 Pawelek, J.M., and Chakraborty, A.K. (1998). The enzymology of melanogenesis. (Oxford University Press), pp. 391-400.
16 Seong, I., Min, H.J., Lee, J.H., Yeo, C.Y., Kang, D.M., Oh, E.S., Hwang, E.S., and Kim, J. (2012). Sox10 controls migration of B16F10 melanoma cells through multiple regulatory target genes. PLoS One 7, e31477.   DOI   ScienceOn
17 Brennan, C.M., and Steitz, J.A. (2001). HuR and mRNA stability. Cell. Mol. Life Sci. 58, 266-277.   DOI
18 Ahn, S.J., Koketsu, M., Ishihara, H., Lee, S.M., Ha SK, Lee KH, Kang, T.H., and Kima, S.Y. (2006). Regulation of melanin synthesis by selenium-containing carbohydrates. Chem. Pharm. Bull. 54, 281-286.   DOI   ScienceOn
19 Bertolotto, C., Abbe, P., Hemesath, T.J., Bille, K., Fisher, D.E., Ortonne, J.P., and Ballotti, R. (1998). Microphthalmia gene product as a signal transducer in cAMP-induced differentiation of melanocytes. J. Cell Biol. 142, 827-835.   DOI
20 Boissy, R.E. (2003). Melanosome transfer to and translocation in the keratinocyte. Exp. Dermatol. 12, 5-12.   DOI   ScienceOn
21 Brenner, M., and Hearing, V.J. (2008). The protective role of melanin against UV damage in human skin. Photochem. Photobiol. 84, 539-549.   DOI   ScienceOn
22 Busca, R., Bertolotto, C., Ortonne, J.P., and Ballotti, R. (1996). Inhibition of the phosphatidylinositol 3-kinase/p70(S6)-kinase pathway induces B16 melanoma cell differentiation. J. Biol. Chem. 271, 31824-31830.   DOI   ScienceOn
23 Chen, C.Y., Xu, N., and Shyu, A.B. (2002). Highly selective actions of HuR in antagonizing AU-rich element-mediated mRNA destabilization. Mol. Cell. Biol. 22, 7268-7278.   DOI
24 Unver, N., Freyschmidt-Paul, P., Horster, S., Wenck, H., Stab, F., Blatt, T., and Elsasser, H.P. (2006). Alterations in the epidermaldermal melanin axis and factor XIIIa melanophages in senile lentigo and ageing skin. Br. J. Dermatol. 155, 119-128.   DOI   ScienceOn
25 Sharma, P., Dube, D., Singh, A., Mishra, B., Singh, N., Sinha, M., Dey, S., Kaur, P., Mitra, D.K., et al. (2011). Structural basis of recognition of pathogen-associated molecular patterns and inhibition of proinflammatory cytokines by camel peptidoglycan recognition protein. J. Biol. Chem. 286, 16208-16217.   DOI   ScienceOn
26 Shen, T., Heo, S.I., and Wang, M.H. (2012). 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. 199, 106-111.   DOI   ScienceOn
27 Su, T.R., Lin, J.J., Tsai, C.C., Huang, T.K., Yang, Z.Y., Wu, M.O., Zheng, Y.Q., Su, C.C., and Wu, Y.J. (2013). I 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. Int. J. Mol. Sci. 14, 20443-20458.   DOI
28 Wen, F., Shen, A., Shanas, R., Bhattacharyya, A., Lian, F., Hostetter, G., and Shi, J. (2010). Higher expression of the heter- ogeneous nuclear ribonucleoprotein k in melanoma. Ann. Surg. Oncol. 17, 2619-2627.   DOI   ScienceOn
29 Xu, W., Gong, L., Haddad, M.M., Bischof, O., Campisi, J., Yeh, E.T., and Medrano, E.E. (2000). Regulation of microphthalmiaassociated transcription factor MITF protein levels by association with the ubiquitin-conjugating enzyme hUBC9. Exp. Cell Res. 255, 135-143.   DOI   ScienceOn
30 Yagi, A., Kanbara, T., and Morinobu, N. (1987). Inhibition of mushroom- tyrosinase by aloe extract. Planta Med. 53, 517-519.   DOI   ScienceOn
31 Englaro, W., Bertolotto, C., Busca, R., Brunet, A., Pages, G., Ortonne, J.P., and Ballotti, R. (1998). Inhibition of the mitogenactivated protein kinase pathway triggers B16 melanoma cell differentiation. J. Biol. Chem. 273, 9966-9970.   DOI   ScienceOn
32 Chung, S.Y., Seo, Y.K., Park, J.M., Seo, M.J., Park, J.K., Kim, J.W., and Park, C.S. (2009). Fermented rice bran downregulates MITF expression and leads to inhibition of alpha-MSH-induced melano-genesis in B16F1 melanoma. Biosci. Biotechnol. Biochem. 73, 1704-1710.   DOI   ScienceOn
33 Costin, G.E., and Hearing, V.J. (2007). Human skin pigmentation: melanocytes modulate skin color in response to stress. FASEB J. 21, 976-994.   DOI   ScienceOn
34 Draelos, Z.D. (2007). Skin lightening preparations and the hydroquinone controversy. Dermatol. Ther. 20, 308-313.   DOI   ScienceOn
35 Hemesath, T.J., Price, E.R., Takemoto, C., Badalian, T., and Fisher, D.E. (1998). MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature 391, 298-301.   DOI   ScienceOn
36 Hennessy, B.T., Smith, D.L., Ram, P.T., Lu, Y., and Mills, G.B. (2005). Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat. Rev. Drug Discov. 4, 988-1004.   DOI   ScienceOn
37 Iozumi, K., Hoganson, G.E., Pennella, R., Everett, M.A., and Fuller, B.B. (1993). Role of tyrosinase as the determinant of pigmentation in cultured human melanocytes. J. Invest. Dermatol. 100, 806-811.   DOI   ScienceOn
38 Isaac, G. (2002). Role of lipoteichoic acid in infection and inflammation. LANCET Infect. Dis. 2, 171-179.   DOI   ScienceOn
39 Zeng, R.Z., Kim, H.G., Kim, N.R., Lee, H.Y., Jung, B.J., Ko, M.Y., Lee, S.Y., and Chung, D.K. (2010). Protein expression changes in human monocytic THP-1 cells treated with lipoteichoic acid from Lactobacillus plantarum and Staphylococcus aureus. Mol. Cells 6, 585-594.