CC BY-NC-ND 4.0 · Planta Medica International Open 2020; 7(01): e34-e44
DOI: 10.1055/a-1141-0151
Original Papers
Eigentümer und Copyright ©Georg Thieme Verlag KG 2020

Tara Tannin Regulates Pigmentation by Modulating Melanogenesis Enzymes and Melanosome Transport Proteins Expression

Myra O. Villareal
1   Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba City, Ibaraki, Japan
2   Alliance for Research on the Mediterranean and North Africa (ARENA), University of Tsukuba, Tsukuba City, Ibaraki, Japan
3   School of Integrative and Global Majors (SIGMA), University of Tsukuba, Tsukuba City, Ibaraki Japan
,
Thanyanan Chaochaiphat
3   School of Integrative and Global Majors (SIGMA), University of Tsukuba, Tsukuba City, Ibaraki Japan
4   Nano Innovation Laboratories Co., Ltd., Ninomiyamachi, Nakagun, Kanagawa, Japan
,
Meriem Bejaoui
3   School of Integrative and Global Majors (SIGMA), University of Tsukuba, Tsukuba City, Ibaraki Japan
,
Kozo Sato
4   Nano Innovation Laboratories Co., Ltd., Ninomiyamachi, Nakagun, Kanagawa, Japan
,
Hiroko Isoda
1   Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba City, Ibaraki, Japan
2   Alliance for Research on the Mediterranean and North Africa (ARENA), University of Tsukuba, Tsukuba City, Ibaraki, Japan
3   School of Integrative and Global Majors (SIGMA), University of Tsukuba, Tsukuba City, Ibaraki Japan
› Institutsangaben
Weitere Informationen

Publikationsverlauf

received 02. Juli 2019

accepted 10. März 2020

Publikationsdatum:
15. April 2020 (online)

Abstract

The skin color is imparted by the pigment melanin produced in the melanosomes of melanocytes, through the catalytic action of melanogenesis enzymes tyrosinase, tyrosinase-related protein 1, and dopachrome tautomerase. Disruptions in the melanogenesis process may result to hypopigmentation, as observed in cutaneous postinflammatory conditions. Here, the bioactivity of tara tannin, specifically on melanogenesis, was evaluated in vitro using human epidermal melanocytes (HEM) and B16F10 murine melanoma cells in order to determine the possibility that it may be used as a treatment against hypopigmentation. The melanin content of tara tannin-treated B16F10 cells and the expression level of melanogenesis enzymes and melanosome transport proteins were determined. To elucidate the underlying mechanism of tara tannin’s effect on melanogenesis, DNA microarray analysis was performed. Tara tannin significantly increased melanogenesis in both murine and human pigment cell models by upregulating melanogenesis-associated enzymes’ (tyrosinase, tyrosinase-related protein 1, and dopachrome tautomerase) protein and mRNA expression levels, as well as the melanosome transport proteins (myosin Va and RAB27A) expression, both attributed to increased microphthalmia-associated transcription factor (MITF) expression. Global gene expression analysis results revealed the modulation of genes (p≤0.05; fold-change ≥2.0 and ≤−2.0) that are under the transcriptional regulation of MITF and genes relevant for MAPK signaling, metabolic pathways, and cell cycle. Tara tannin has a significant effective melanogenesis-promoting effect, making it a potential therapeutic agent against hypopigmentation disorders. This is the first report on the melanogenesis regulatory effect of tara tannin in vitro.

Supporting information

 
  • References

  • 1 Jy Lin, De Fisher. Melanocyte biology and skin pigmentation. Nature 2007; 445: 843-850
  • 2 Hirobe T, Enami H. Melanoblast but not melanocytes decrease in number in human epidermis of idiopathic guttate hypomelanosis. Dermatol Sinica 2018; 36: 131-135
  • 3 Ganesan AK, Ho H, Bodemann B, Petersen S, Aruri J, Koshy S, Richardson Z. et al. Genome-wide siRNA-based functional genomics of pigmentation identifies novel genes and pathways that impact melanogenesis in human cells. PLoS Genet 2008; 4: e1000298
  • 4 Barrenäs M-L, Lindgren F. The influence of inner ear melanin on susceptibility to TTS in humans. Scand Audiol 1990; 19: 97-102
  • 5 Herrling T, Jung K, Fuchs J. The role of melanin as protector against free radicals in skin and its role as free radical indicator in hair. Spectrochim Acta Part A Mol Biomol Spectrosc 2008; 69: 1429-1435
  • 6 Hearing V, Tsukamoto K. Enzymatic control of pigmentation in mammals. FASEB J. 1991; 5: 2902-2909
  • 7 Duval C, Chagnoleau C, Pouradier F, Sextius P, Condom E, Bernerd F. Human skin model containing melanocytes: essential role of keratinocyte growth factor for constitutive pigmentation—functional response to α-melanocyte stimulating hormone and forskolin. Tissue Eng Part C Methods 2012; 18: 947-957
  • 8 Wasmeier C, Hume AN, Bolasco G, Seabra MC. Melanosomes at a glance. J Cell Sci 2008; 121: 3995-3999
  • 9 Gaggioli C, Buscà R, Abbe P, Ortonne J-P, Ballotti R. Microphthalmia-associated transcription factor (MITF) is required but is not sufficient to induce the expression of melanogenic genes. Pigment Cell Res 2003; 16: 374-382
  • 10 Steingrímsson E, Copeland NG, Jenkins NA. Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet 2004; 38: 365-411
  • 11 Khaled M, Larribere L, Bille K, Aberdam E, Ortonne JP, Balloti R, Bertolotto C. Glycogen synthase kinase 3beta is activated by cAMP and plays an active role in the regulation of melanogenesis. J Biol Chem 2002; 277: 33690-33697
  • 12 Villareal MO, Han J, Matsuyama K, Sekii Y, Smaoui A, Shigemori H, Isoda H. Lupenone from Erica multiflora leaf extract stimulates melanogenesis in B16 murine melanoma cells through the inhibition of ERK1/2 activation. Planta Med. 2013; 79: 236-243
  • 13 Matsuyama K, Villareal MO, El Omri A, Elyes Kchouk M, Han J, Isoda H. Effect of Tunisian Capparis spinosa L. extract on melanogenesis in B16 murine melanoma cells. J Nat Med 2009; 63: 468-472
  • 14 Villareal MO, Kume S, Neffati M, Isoda H. Upregulation of Mitf by Phenolic compounds-rich cymbopogon schoenanthus treatment promotes melanogenesis in B16 melanoma cells and human epidermal melanocytes. BioMed Research International 2017; 2017: 1-11
  • 15 Mo Villareal, Han J, Ikuta K, Isoda H. Mechanism of Mitf inhibition and morphological differentiation effects of hirsein A on B16 melanoma cells revealed by DNA microarray. J Dermatol Sci 2012; 67: 26-36
  • 16 Clifford MN, Stoupi S, Kuhnert N. Profiling and characterization by LC-MSn of the galloylquinic acids of green tea, tara tannin, and tannic acid. J Agric Food Chem 2007; 55: 2797-2807
  • 17 Deschamps AM, Lebeault J-M. Production of gallic acid from tara tannin by bacterial strains. Biotechnol Lett 1984; 6: 237-242
  • 18 Bellotti N, del Amo B, Romagnoli R. Tara tannin a natural product with antifouling coating application. Progress Org. Coatings 2012; 74: 411-417
  • 19 Bellotti N, del Amo B, Romagnoli R. Caesalpinia spinosa tannin derivaties for antifouling formulations. Procedia Materials Sci 2012; 1: 259-265
  • 20 Hunt N, McHale S. The psychological impact of alopecia. BMJ Br Med J 2005; 331: 951-953
  • 21 Nagata H, Takekoshi S, Takeyama R, Homma T, Yoshiyuki Osamura R. Quercetin enhances melanogenesis by increasing the activity and synthesis of tyrosinase in human melanoma cells and in normal human melanocytes. Pigment Cell Res 2004; 17: 66-73
  • 22 Kumagai A, Horike N, Satoh Y, Uebi T, Sasaki T, Itoh Y, Hirata Y. et al. A potent inhibitor of SIK2, 3, 3′, 7-trihydroxy-4′-methoxyflavon (4′-o-methylfisetin), promotes melanogenesis in B16F10 melanoma cells. PLoS One 2011; 6: e26148
  • 23 Haslam E, Hawroth D, Jones K, Rogers HJ. Gallotannins. Part 1. Introduction: and the fractionation of tannase. J Chem Soc 1961; 0: 1929-1935
  • 24 Horler DF, Nursten HE. The tannins of tara, Caesalpinia spinosa (mol) kuntze. J Chem Soc 1961; 0: 3786-3792
  • 25 Aouf C, Benyahya S, Esnouf A, Caillol S, Boutevin B, Fulcard H. Tara tannins as phenolic precursors of thermosetting apoxy. Eur Polymer J 2014; 55: 186-198
  • 26 Garro Galvez JM, Riedl B, Conner AH. Analytical studies on tara tannins. Holzforschung 1997; 51: 235-243
  • 27 Su TR, Lin JJ, Tsai CC, Huang TK, Yang ZY, Wu MO, Zheng YQ. et al. Inhibition of melanogenesis by gallic acid: possible involvement of the PI3K/Akt, MEK/ERK and Wnt/beta-catenin signaling pathways in B16F10. cells. J Mol Sci 2013; 14: 20443-20458
  • 28 Shimogaki H, Tanaka Y, Tamai H, Masuda M. In vitro and in vivo evaluation of ellagic acid on melanogenesis inhibition. Int J Cosmet Sci 2000; 22: 291-303
  • 29 Bahadoran P, Aberdam E, Mantoux F, Buscà R, Bille K, Yalman N, de Saint-Basile G. et al. Rab27a: A key to melanosome transport in human melanocytes. J Cell Biol 2001; 152: 843-850
  • 30 Wu X, Bowers B, Rao K, Wei Q, Hammer JA. Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function in vivo . J Cell Biol 1998; 143: 1899-1918
  • 31 Sheets L, Ransom DG, Mellgren EM, Johnson SL, Schnapp BJ. Zebrafish melanophilin facilitates melanosome dispersion by regulating dynein. Curr Biol 2007; 17: 1721-1734
  • 32 Seabra MC, Coudrier E. RabGT Pases and myosin motors in organelle motility. Traffic 2004; 5: 393-399
  • 33 García-Borrón JC, Sánchez-Laorden BL, Jiménez-Cervantes C. Melanocortin-1 receptor structure and functional regulation. Pigment Cell Res 2005; 18: 393-410
  • 34 Chiaverini C, Beuret L, Flori E, Busca R, Abbe P, Bille K, Bahadoran P. et al. Microphthalmia-associated transcription factor regulates Rab27a gene expression and controls melanosome transport. J Biol Chem 2008; 283: 12635-12642
  • 35 Vachtenheim J, Borovansky J. “Transcription physiology” of pigment formation in melanocytes: Central role of MITF. Exp Dermatol 2010; 19: 617-627
  • 36 Lee E, Han J, Kim K, Choi H, Cho EG, Lee TR. CXCR7 mediates SDF1-induced melanocyte migration. Pigment Cell Melanoma Res 2013; 26: 58-66
  • 37 Laurette P, Strub T, Koludrovic D, Keime C, Le Gras S, Seberg H, Van Otterloo E. et al. Transcription factor MITF and remodeller BRG1 define chromatin organisation at regulatory elements in melanoma cells. eLife 2015; 4: e06857
  • 38 Han J, Kraft P, Nan H, Guo Q, Chen C, Qureshi A, Hankinson SE. et al. A genome-wide association study identifies novel alleles associated with hair color and skin pigmentation. PLoS Genet 2008; 4: e1000074
  • 39 Villareal MO, Kume S, Neffati M, Isoda H. Upregulation of Mitf by phenolic compounds-rich cymbopogon schoenanthus treatment promotes melanogenesis in B16 melanoma cells and human epidermal melanocytes. BioMed Research International 2017; 2017: 1-11
  • 40 Hong SH, Sim MJ, Kim YC. Melanogenesis-promoting effects of Rhynchosia nulubilis and Rhynchosia volubilis ethanol extracts in melan-a cells. Toxicol Res 2016; 32: 141-147
  • 41 Venter P, Pasch H, de Villiers A. Comprehensive analysis of tara tannins by reversed-phase and hydrophilic interaction chromatography coupled to ion mobility and high-resolution mass spectrophotometry. Anal Bioanak Chem 2019; 411: 6329-6341