Role of NADPH Oxidase-mediated Generation of Reactive Oxygen Species in the Apigenin-induced Melanogenesis in B16 Melanoma Cells

B16 흑색종세포에서 아피제닌에 의한 멜라닌 합성에 미치는 NADPH 산화효소-유래 활성산소종의 역할

  • Received : 2011.11.30
  • Accepted : 2011.12.15
  • Published : 2011.12.31

Abstract

Previously, we have reported that apigenin, a natural flavonoid found in a variety of vegetables and fruits, stimulated melanogenesis through the activation of $K^+-Cl^-$-cotransport (KCC) in B16 melanoma cells. In this study we investigated the possible involvement of reactive oxygen species (ROS) in the mechanism of apigenin-induced melanogenesis in B16 cells. Apigenin elevated intracellular ROS level in a dose-dependent manner. Treatment with various inhibitors of NADPH oxidase, diphenylene iodonium (DPI), apocynin (Apo) and neopterine (NP) significantly inhibited both the generation of ROS and melanogenesis induced by apigenin. In addition these inhibitors profoundly inhibited apigenin-induced $Cl^-$-dependent $K^+$ efflux, a hallmark of KCC activity. However, the apigenin-induced ROS generation was not significantly affected by treatment with a specific KCC inhibitor R-(+)-[(2-n-butyl-6,7-dichloro-2-cyclopentyl-2,3-dihydro-1-oxo-1H-inden-5-yl)oxy]acetic acid (DIOA). These results indicate that the ROS production may be a upstream regulator of the apigenin-induced KCC stimulation, and in turn, melanogenesis in the B16 cells. Taken together, these results suggest that the NADPH oxidase-mediated ROS production may play an important role in the apigenin-induced melanogenesis in B16 cells. These results further suggest that NADPH oxidase may be a good target for the management of hyperpigmentation disorders.

Keywords

References

  1. Seiberg, M. : Keratinocyte-melanocyte interaction during melanosome transfer. Pigment Cell Res. 14, 236 (2001). https://doi.org/10.1034/j.1600-0749.2001.140402.x
  2. Coelho, S. G., Choi, W., Brenner, M., Miyamura, Y., Yamaguchi, Y., Wolber, R., Smuda, C., Batzer, J., Kolbe, L., Ito, S., Wakamatsu, K., Zmudzka, B. Z., Beer, J. Z., Miller, S. A. and Hearing, V. J. : Short- and long-term effects of UV radiation on the pigmentation of human skin. J. Investig. Dermatol. Symp. Proc. 14, 32 (2009).
  3. Kondo, T. and Hearing, V. J. : Update on the regulation of mammalian melanocyte function and skin pigmentation. Expert Rev. Dermatol. 6, 97 (2011). https://doi.org/10.1586/edm.10.70
  4. Wang, H. M., Chen, C. Y. and Wen, Z. H. : Identifying melanogenesis inhibitors from Cinnamomum subavenium with in vitro and in vivo screening systems by targeting the human tyrosinase. Exp. Dermatol. 20, 242 (2011). https://doi.org/10.1111/j.1600-0625.2010.01161.x
  5. Peterson, J. and Dwyer, J. : Flavonoids: dietary occurrence and biochemical activity. Nutr. Res. 18, 1995 (1988).
  6. Li, R. R., Pang, L. L., Du, Q., Shi, Y., Dai, W. J. and Yin, K. S. : Apigenin inhibits allergen-induced airway inflammation and switches immune response in a murine model of asthma. Immunopharmacol. Immunotoxicol. 32, 364 (2010). https://doi.org/10.3109/08923970903420566
  7. Shukla, S. and Gupta, S. : Apigenin: a promising molecule for cancer prevention. Pharm. Res. 27, 962 (2010). https://doi.org/10.1007/s11095-010-0089-7
  8. Long, X., Fan, M., Bigsby, R. M. and Nephew, K. P. : Apigenin inhibits antiestrogen-resistant breast cancer cell growth through estrogen receptor-a-dependent and estrogen receptora-independent mechanisms. Mol. Cancer Ther. 7, 2096 (2008). https://doi.org/10.1158/1535-7163.MCT-07-2350
  9. Valdameri, G., Trombetta-Lima, M., Worfel, P. R., Pires, A. R., Martinez, G. R., Noleto, G. R., Cadena, S. M., Sogayar, M. C., Winnischofer, S. M. and Rocha, M. E. : Involvement of catalase in the apoptotic mechanism induced by apigenin in HepG2 human hepatoma cells. Chem. Biol. Interact. 193, 180 (2011). https://doi.org/10.1016/j.cbi.2011.06.009
  10. Shukla, S. and Gupta, S. : Apigenin-induced prostate cancer cell death is initiated by reactive oxygen species and p53 activation. Free Radic. Biol. Med. 44, 1833 (2008). https://doi.org/10.1016/j.freeradbiomed.2008.02.007
  11. Kim, M. H., Jeong, C. S., Yoon, H. R., Kim, G. H. and Lee, Y. S. : Involvement of $K^{+}$-$Cl^{-}$-cotransport in the apigenin-Induced generation of reactive oxygen species in IMR-32 human neuroblastoma cells. J. Appl. Pharmacol. 14, 137 (2006).
  12. Cossins, A. R. and Gibson, J. S. : Volume-sensitive transport systems and volume homeostasis in vertebrate red blood cells. J. Exp. Biol. 200, 343 (1997).
  13. Amlal, H., Paillard, M. and Bichara, M. : $Cl^{-}$-dependent $NH_{4}^{+}$ transport mechanisms in medullary thick ascending limb cells. Am. J. Physiol. 267, C1607 (1994). https://doi.org/10.1152/ajpcell.1994.267.6.C1607
  14. Perry, P. B. and O'Neill, W. C. : Swelling-activated K fluxes in vascular endothelial cells: volume regulation via K-Cl cotransport and K channels. Am. J. Physiol. 265, C763 (1993). https://doi.org/10.1152/ajpcell.1993.265.3.C763
  15. Adragna, N. C., White, R. E., Orlov, S. N. and Lauf, P. K. : KCl cotransport in vascular smooth muscle and erythrocytes: possible implication in vasodilation. Am. J. Physiol. 278, C381 (2000). https://doi.org/10.1152/ajpcell.2000.278.2.C381
  16. Yan, G. X., Chen, J., Yamada, K. A., Kleber, A. G. and Corr, P. B. : Contribution of shrinkage of extracellular space to extracellular $K^{+}$ accumulation in myocardial ischaemia of the rabbit. J. Physiol. (London) 490, 215 (1996). https://doi.org/10.1113/jphysiol.1996.sp021137
  17. Weil-Maslansky, E., Gutman, Y. and Sasson, S. : Insulin activates furosemide-sensitive $K^{+}$ and $Cl^{-}$ uptake system in BC3H1 cells. Am. J. Physiol. 267, C932 (1994). https://doi.org/10.1152/ajpcell.1994.267.4.C932
  18. Rivera, C., Voipio, J., Payne, J. A., Ruusuvuori, E., Latineen, H., Lamsa, K., Pirvola, U., Saarma, M. and Kaila, K. : The $K^{+}$/$Cl^{-}$ co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251 (1999). https://doi.org/10.1038/16697
  19. Lauf, P. K., Bauer, J., Adragna, N. C., Fujise, H., Zade-Oppen, A. M., Ryu, K. H. and Delpire, E. : Erythrocyte K-Cl cotransport: properties and regulation. Am. J. Physiol. 263, C917 (1992). https://doi.org/10.1152/ajpcell.1992.263.5.C917
  20. Ellison, D. H., Velazquez, H. and Wright, F. S. : Stimulation of distal potassium secretion by low lumen chloride in the presence of barium. Am. J. Physiol. 248, F638 (1985).
  21. Kim, J. A., Kang, Y. S. and Lee, Y. S. : Involvement of $K^{+}$- $Cl^{-}$-cotransport in the apoptosis induced by N-ethylmaleimide in HepG2 human hepatoblastoma cells. Eur. J. Pharmacol. 418, 1 (2001). https://doi.org/10.1016/S0014-2999(01)00861-5
  22. Lee, Y. S. : Role of $K^{+}$-$Cl^{-}$-cotransporter in the apigenininduced stimulation of melanogenesis in B16 melanoma cells. Yakhak Hoeji 52, 500 (2008).
  23. Babior, B. M. : The respiratory burst oxidase. Curr. Opin. Hematol. 2, 55 (1995). https://doi.org/10.1097/00062752-199502010-00008
  24. Jones, S. A., O'Donnell, V. B., Wood, J. D., Broughton, J. P., Hughes, E. J. and Jones, O. T. : Expression of phagocyte NADPH oxidase components in human endothelial cells. Am. J. Physiol. 271, H1626 (1996).
  25. Marshall, C., Mamary, A. J., Verhoeven, A. J. and Marshall, B. E. : Pulmonary artery NADPH oxidase is activated in hypoxic pulmonary vasoconstriction. Am. J. Respir. Cell Mol. Biol. 15, 633 (1996). https://doi.org/10.1165/ajrcmb.15.5.8918370
  26. Youngson, C., Nurse, C., Yeger, H., Curnutte, J. T., Vollmer, C., Wong, V. and Cutz, E. : Immunocytochemical localization on $O_{2}$-sensing protein (NADPH oxidase) in chemoreceptor cells. Microsc. Res. Tech. 37, 101 (1997). https://doi.org/10.1002/(SICI)1097-0029(19970401)37:1<101::AID-JEMT10>3.0.CO;2-V
  27. Kummer, W. and Acker, H. : Immunohistochemical demonstration of four subunits of neutrophil NAD(P)H oxidase in type I cells of carotid body. J. Appl. Physiol. 78, 1904 (1995). https://doi.org/10.1152/jappl.1995.78.5.1904
  28. Zhao, Y., Liu, J. and McMartin, K. E. : Inhibition of NADPH oxidase activity promotes differentiation of B16 melanoma cells. Oncol. Rep. 19, 1225 (2008).
  29. Babior, B. M. : NADPH oxidase: an update. Blood 93, 1464 (1999).
  30. Choi, S. I., Jeong, C. S., Cho, S. Y. and Lee, Y. S. : Mechanism of apoptosis induced by apigenin in HepG2 human hepatoma cells: involvement of reactive oxygen species generated by NADPH oxidase. Arch. Pharm. Res. 30, 1328 (2007). https://doi.org/10.1007/BF02980274
  31. Kim, J. A. and Lee, Y. S. : Role of reactive oxygen species generated by NADPH oxidase in the mechanism of activation of $K^{+}$-$Cl^{-}$-cotransport by N-ethylmaleimide in HepG2 human hepatoma cells. Free Radic. Res. 35, 43 (2001). https://doi.org/10.1080/10715760100300581
  32. Queen, B. L. and Tollefsbol, T. O. : Polyphenols and aging. Curr. Aging Sci. 3, 34 (2010). https://doi.org/10.2174/1874609811003010034
  33. Ullah, M. F., Ahmad, A., Zubair, H., Khan, H. Y., Wang, Z., Sarkar, F. H. and Hadi, S. M. : Soy isoflavone genistein induces cell death in breast cancer cells through mobilization of endogenous copper ions and generation of reactive oxygen species. Mol. Nutr. Food Res. 55, 553 (2011). https://doi.org/10.1002/mnfr.201000329
  34. Ago, T., Kuroda, J., Kamouchi, M., Sadoshima, J. and Kitazono, T. : Pathophysiological roles of NADPH oxidase/nox family proteins in the vascular system. Review and perspective. Circ. J. 75, 1791 (2011). https://doi.org/10.1253/circj.CJ-11-0388
  35. Crestani, B., Besnard, V. and Boczkowski, J. : Signalling pathways from NADPH oxidase-4 to idiopathic pulmonary fibrosis. Int. J. Biochem. Cell Biol. 43, 1086 (2011). https://doi.org/10.1016/j.biocel.2011.04.003
  36. Tojo, A., Asaba, K. and Onozato, M. L. : Suppressing renal NADPH oxidase to treat diabetic nephropathy. Expert Opin. Ther. Targets 11, 1011 (2007). https://doi.org/10.1517/14728222.11.8.1011
  37. Kim, Y. J., Kang, K. S. and Yokozawa, T. : The anti-melanogenic effect of pycnogenol by its anti-oxidative actions. Food Chem. Toxicol. 46, 2466 (2008). https://doi.org/10.1016/j.fct.2008.04.002
  38. Ohguchi, K., Akao, Y. and Nozawa, Y. : Stimulation of melanogenesis by the citrus flavonoid naringenin in mouse B16 melanoma cells. Biosci. Biotechnol. Biochem. 70, 1499 (2006). https://doi.org/10.1271/bbb.50635
  39. Busca, R. and Ballotti, R. : Cyclic AMP a key messenger in the regulation of skin pigmentation. Pigment. Cell Res. 13, 60 (2000). https://doi.org/10.1034/j.1600-0749.2000.130203.x
  40. Dong, Y., Wang, H., Cao, J., Ren, J., Fan, R., He, X., Smith, G. W. and Dong, C. : Nitric oxide enhances melanogenesis of alpaca skin melanocytes in vitro by activating the MITF phosphorylation. Mol. Cell. Biochem. 352, 255 (2011). https://doi.org/10.1007/s11010-011-0761-1
  41. Valencia, A. and Kochevar, I. E. : Nox1-based NADPH oxidase is the major source of UVA-induced reactive oxygen species in human keratinocytes. J. Invest. Dermatol. 128, 214 (2008). https://doi.org/10.1038/sj.jid.5700960
  42. Ginger, R. S., Askew, S. E., Ogborne, R. M., Wilson, S., Ferdinando, D., Dadd, T., Smith, A. M., Kazi, S., Szerencsei, R. T., Winkfein, R. J., Schnetkamp, P. P. and Green, M. R. : SLC24A5 encodes a trans-Golgi network protein with potassium-dependent sodium-calcium exchange activity that regulates human epidermal melanogenesis. J. Biol. Chem. 283, 5486 (2008). https://doi.org/10.1074/jbc.M707521200
  43. Han, H. Y., Lee, J. R., Xu, W. A., Hahn, M. J., Yang, J. M. and Park, Y. D. : Effect of $Cl^{-}$ on tyrosinase: complex inhibition kinetics and biochemical implication. J. Biomol. Struct. Dyn. 25, 165 (2007). https://doi.org/10.1080/07391102.2007.10507165
  44. Fu, X., Beer, D. G., Behar, J., Wands, J., Lambeth, D. and Cao, W. : cAMP-response element-binding protein mediates acidinduced NADPH oxidase NOX5-S expression in Barrett esophageal adenocarcinoma cells. J. Biol. Chem. 281, 20368 (2006). https://doi.org/10.1074/jbc.M603353200
  45. Craige, S. M., Chen, K., Pei, Y., Li, C., Huang, X., Chen, C., Shibata, R., Sato, K., Walsh, K. and Keaney, J. F. Jr. : NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation 124, 731 (2011). https://doi.org/10.1161/CIRCULATIONAHA.111.030775
  46. Di Fulvio, M., Lauf, P. K. and Adragna, N. C. : Nitric oxide signaling pathway regulates potassium chloride cotransporter-1 mRNA expression in vascular smooth muscle cells. J. Biol. Chem. 276, 44534 (2001). https://doi.org/10.1074/jbc.M104899200