Toxicological Research

  • 제34권4호
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  • Pages.333-341
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  • 2018
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  • 1976-8257(pISSN)
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  • 2234-2753(eISSN)
한국독성학회 (Korean Society of Toxicology & Korea Environmental Mutagen Society)
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Ferulate, an Active Component of Wheat Germ, Ameliorates Oxidative Stress-Induced PTK/PTP Imbalance and PP2A Inactivation

  • Koh, Eun Mi (Bioanalytical and Immunoanalytical Research Group, Korea Institute of Toxicology) ;
  • Lee, Eun Kyeong (Bioanalytical and Immunoanalytical Research Group, Korea Institute of Toxicology) ;
  • Song, Chi Hun (Bioanalytical and Immunoanalytical Research Group, Korea Institute of Toxicology) ;
  • Song, Jeongah (Animal Model Research Center, Korea Institute of Toxicology) ;
  • Chung, Hae Young (Molecular Inflammation Research Center for Aging Intervention (MRCA), College of Pharmacy, Pusan National University) ;
  • Chae, Chang Hoon (Celldi) ;
  • Jung, Kyung Jin (Bioanalytical and Immunoanalytical Research Group, Korea Institute of Toxicology)
  • 투고 : 2017.08.25
  • 심사 : 2018.07.04
  • 발행 : 2018.10.15
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초록

Ferulate is a phenolic compound abundant in wheat germ and bran and has been investigated for its beneficial activities. The aim of the present study is to evaluate the efficacy of ferulate against the oxidative stress-induced imbalance of protein tyrosine kinases (PTKs), protein tyrosine phosphatases (PTPs), and serine/threonine protein phosphatase 2A (PP2A), in connection with our previous finding that oxidative stress-induced imbalance of PTKs and PTPs is linked with proinflammatory nuclear factor-kappa B $(NF-{\kappa}B)$ activation. To test the effects of ferulate on this process, we utilized two oxidative stress-induced inflammatory models. First, YPEN-1 cells were pretreated with ferulate for 1 hr prior to the administration of 2,2'-Azobis(2-methylpropionamidine) dihydrochloride (AAPH). Second, 20-month-old Sprague-Dawley rats were fed ferulate for 10 days. After ferulate treatment, the activities of PTKs, PTPs, and PP2A were measured because these proteins either directly or indirectly promote $NF-{\kappa}B$ activation. Our results revealed that in YPEN-1 cells, ferulate effectively suppressed AAPH-induced increases in reactive oxygen species (ROS) and $NF-{\kappa}B$ activity, as well as AAPH-induced PTK activation. Furthermore, ferulate also inhibited AAPH-induced PTP and PP2A inactivation. In the aged kidney model, ferulate suppressed aging-induced activation of PTKs and ameliorated aging-induced inactivation of PTPs and PP2A. Thus, herein we demonstrated that ferulate could modulate PTK/PTP balance against oxidative stress-induced inactivation of PTPs and PP2A, which is closely linked with $NF-{\kappa}B$ activation. Based on these results, the ability of ferulate to modulate oxidative stress-related inflammatory processes is established, which suggests that this compound could act as a novel therapeutic agent.

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참고문헌

  1. Tee-ngam, P., Nunant, N., Rattanarat, P., Siangproh, W. and Chailapakul, O. (2013) Simple and rapid determination of ferulic acid levels in food and cosmetic samples using paperbased platforms. Sensors (Basel), 13, 13039-13053. https://doi.org/10.3390/s131013039
  2. Balasubashini, M.S., Rukkumani, R., Viswanathan, P. and Menon, V.P. (2004) Ferulic acid alleviates lipid peroxidation in diabetic rats. Phytother. Res., 18, 310-314. https://doi.org/10.1002/ptr.1440
  3. Sung, J.H., Kim, M.O. and Koh, P.O. (2012) Ferulic acid attenuates the focal cerebral ischemic injury-induced decrease in parvalbumin expression. Neurosci. Lett., 516, 146-150. https://doi.org/10.1016/j.neulet.2012.03.078
  4. Baskaran, N., Manoharan, S., Balakrishnan, S. and Pugalendhi, P. (2010) Chemopreventive potential of ferulic acid in 7,12-dimethylbenz[a]anthracene-induced mammary carcinogenesis in Sprague-Dawley rats. Eur. J. Pharmacol., 637, 22-29. https://doi.org/10.1016/j.ejphar.2010.03.054
  5. Fong, Y., Tang, C.C., Hu, H.T., Fang, H.Y., Chen, B.H., Wu, C.Y., Yuan, S.S., Wang, H.D., Chen, Y.C., Teng, Y.N. and Chiu, C.C. (2016) Inhibitory effect of trans-ferulic acid on proliferation and migration of human lung cancer cells accompanied with increased endogenous reactive oxygen species and beta-catenin instability. Chin. Med., 11, 45. https://doi.org/10.1186/s13020-016-0116-7
  6. Liang, Q., Ju, Y., Chen, Y., Wang, W., Li, J., Zhang, L., Xu, H., Wood, R.W., Schwarz, E.M., Boyce, B.F., Wang, Y. and Xing, L. (2016) Lymphatic endothelial cells efferent to inflamed joints produce iNOS and inhibit lymphatic vessel contraction and drainage in TNF-induced arthritis in mice. Arthritis Res. Ther., 18, 62. https://doi.org/10.1186/s13075-016-0963-8
  7. Yang, H., Qu, Z., Zhang, J., Huo, L., Gao, J. and Gao, W. (2016) Ferulic acid ameliorates memory impairment in dgalactose-induced aging mouse model. Int. J. Food Sci. Nutr., 67, 806-817. https://doi.org/10.1080/09637486.2016.1198890
  8. Navarrete, S., Alarcon, M. and Palomo, I. (2015) Aqueous extract of Tomato (Solanum lycopersicum L.) and ferulic acid reduce the expression of TNF-alpha and IL-1beta in LPS-activated macrophages. Molecules, 20, 15319-15329. https://doi.org/10.3390/molecules200815319
  9. Lampiasi, N. and Montana, G. (2016) The molecular events behind ferulic acid mediated modulation of IL-6 expression in LPS-activated Raw 264.7 cells. Immunobiology, 221, 486-493. https://doi.org/10.1016/j.imbio.2015.11.001
  10. He, G.Y., Xie, M., Gao, Y. and Huang, J.G. (2015) Sodium ferulate attenuates oxidative stress induced inflammation via suppressing NALP3 and NF-kappaB signal pathway. Sichuan Da Xue Xue Bao Yi Xue Ban, 46, 367-371.
  11. Jung, K.J., Go, E.K., Kim, J.Y., Yu, B.P. and Chung, H.Y. (2009) Suppression of age-related renal changes in NF-kappaB and its target gene expression by dietary ferulate. J. Nutr. Biochem., 20, 378-388. https://doi.org/10.1016/j.jnutbio.2008.04.008
  12. Banning, A. and Brigelius-Flohe, R. (2005) NF-kappaB, Nrf2, and HO-1 interplay in redox-regulated VCAM-1 expression. Antioxid. Redox. Signal., 7, 889-899. https://doi.org/10.1089/ars.2005.7.889
  13. Karin, M. and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol., 18, 621-663. https://doi.org/10.1146/annurev.immunol.18.1.621
  14. Reuter, S., Gupta, S.C., Chaturvedi, M.M. and Aggarwal, B.B. (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic. Biol. Med., 49, 1603-1616. https://doi.org/10.1016/j.freeradbiomed.2010.09.006
  15. Kim, H.J., Jung, K.J., Yu, B.P., Cho, C.G., Choi, J.S. and Chung, H.Y. (2002) Modulation of redox-sensitive transcription factors by calorie restriction during aging. Mech. Ageing. Dev., 123, 1589-1595. https://doi.org/10.1016/S0047-6374(02)00094-5
  16. Jung, K.J., Lee, E.K., Yu, B.P. and Chung, H.Y. (2009) Significance of protein tyrosine kinase/protein tyrosine phosphatase balance in the regulation of NF-kappaB signaling in the inflammatory process and aging. Free Radic. Biol. Med., 47, 983-991. https://doi.org/10.1016/j.freeradbiomed.2009.07.009
  17. Chiarugi, P. (2005) PTPs versus PTKs: the redox side of the coin. Free Radic. Res., 39, 353-364. https://doi.org/10.1080/10715760400027987
  18. Mustelin, T., Vang, T. and Bottini, N. (2005) Protein tyrosine phosphatases and the immune response. Nat. Rev. Immunol., 5, 43-57. https://doi.org/10.1038/nri1530
  19. Frijhoff, J., Dagnell, M., Godfrey, R. and Ostman, A. (2014) Regulation of protein tyrosine phosphatase oxidation in cell adhesion and migration. Antioxid. Redox. Signal., 20, 1994-2010. https://doi.org/10.1089/ars.2013.5643
  20. Barisic, S., Schmidt, C., Walczak, H. and Kulms, D. (2010) Tyrosine phosphatase inhibition triggers sustained canonical serine-dependent NFkappaB activation via Src-dependent blockade of PP2A. Biochem. Pharmacol., 80, 439-447. https://doi.org/10.1016/j.bcp.2010.04.028
  21. Duan, Y., Chen, F., Zhang, A., Zhu, B., Sun, J., Xie, Q. and Chen, Z. (2014) Aspirin inhibits lipopolysaccharide-induced COX-2 expression and PGE2 production in porcine alveolar macrophages by modulating protein kinase C and protein tyrosine phosphatase activity. BMB Rep., 47, 45-50. https://doi.org/10.5483/BMBRep.2014.47.1.089
  22. Jung, K.J., Kim, D.H., Lee, E.K., Song, C.W., Yu, B.P. and Chung, H.Y. (2013) Oxidative stress induces inactivation of protein phosphatase 2A, promoting proinflammatory NFkappaB in aged rat kidney. Free Radic. Biol. Med., 61, 206-217. https://doi.org/10.1016/j.freeradbiomed.2013.04.005
  23. Witt, J., Barisic, S., Schumann, E., Allgower, F., Sawodny, O., Sauter, T. and Kulms, D. (2009) Mechanism of PP2Amediated IKK beta dephosphorylation: a systems biological approach. BMC Syst. Biol., 3, 71. https://doi.org/10.1186/1752-0509-3-71
  24. Guy, G.R., Philp, R. and Tan, Y.H. (1995) Activation of protein kinases and the inactivation of protein phosphatase 2A in tumour necrosis factor and interleukin-1 signal-transduction pathways. Eur. J. Biochem., 229, 503-511. https://doi.org/10.1111/j.1432-1033.1995.tb20491.x
  25. Dobberstein, D. and Bunzel, M. (2010) Separation and detection of cell wall-bound ferulic acid dehydrodimers and dehydrotrimers in cereals and other plant materials by reversed phase high-performance liquid chromatography with ultraviolet detection. J. Agric. Food Chem., 58, 8927-8935. https://doi.org/10.1021/jf101514j
  26. Kern, S.M., Bennett, R.N., Needs, P.W., Mellon, F.A., Kroon, P.A. and Garcia-Conesa, M.T. (2003) Characterization of metabolites of hydroxycinnamates in the in vitro model of human small intestinal epithelium caco-2 cells. J. Agric. Food Chem., 51, 7884-7891. https://doi.org/10.1021/jf030470n
  27. Graf, E. (1992) Antioxidant potential of ferulic acid. Free Radic. Biol. Med., 13, 435-448. https://doi.org/10.1016/0891-5849(92)90184-I
  28. Yuan, J., Ge, K., Mu, J., Rong, J., Zhang, L., Wang, B., Wan, J. and Xia, G. (2016) Ferulic acid attenuated acetaminopheninduced hepatotoxicity though down-regulating the cytochrome P 2E1 and inhibiting toll-like receptor 4 signalingmediated inflammation in mice. Am. J. Transl. Res., 8, 4205-4214.
  29. Sadar, S.S., Vyawahare, N.S. and Bodhankar, S.L. (2016) Ferulic acid ameliorates TNBS-induced ulcerative colitis through modulation of cytokines, oxidative stress, iNOs, COX-2, and apoptosis in laboratory rats. EXCLI J., 15, 482-499.
  30. Huang, H., Hong, Q., Tan, H.L., Xiao, C.R. and Gao, Y. (2016) Ferulic acid prevents LPS-induced up-regulation of PDE4B and stimulates the cAMP/CREB signaling pathway in PC12 cells. Acta Pharmacol. Sin., 37, 1543-1554. https://doi.org/10.1038/aps.2016.88
  31. Wu, Y., Shamoto-Nagai, M., Maruyama, W., Osawa, T. and Naoi, M. (2017) Phytochemicals prevent mitochondrial membrane permeabilization and protect SH-SY5Y cells against apoptosis induced by PK11195, a ligand for outer membrane translocator protein. J. Neural Transm. (Vienna), 124, 89-98.
  32. Ursini, F., Maiorino, M. and Forman, H.J. (2016) Redox homeostasis: The Golden Mean of healthy living. Redox Biol., 8, 205-215. https://doi.org/10.1016/j.redox.2016.01.010
  33. Surh, Y.J., Kundu, J.K., Na, H.K. and Lee, J.S. (2005) Redox-sensitive transcription factors as prime targets for chemoprevention with anti-inflammatory and antioxidative phytochemicals. J. Nutr., 135, 2993S-3001S. https://doi.org/10.1093/jn/135.12.2993S
  34. Schmitz, M.L. and Baeuerle, P.A. (1995) Multi-step activation of NF-kappa B/Rel transcription factors. Immunobiology, 193, 116-127. https://doi.org/10.1016/S0171-2985(11)80534-6
  35. Greten, F.R. and Karin, M. (2004) The IKK/NF-kappaB activation pathway-a target for prevention and treatment of cancer. Cancer Lett., 206, 193-199. https://doi.org/10.1016/j.canlet.2003.08.029
  36. Liu, H.S., Pan, C.E., Liu, Q.G., Yang, W. and Liu, X.M. (2003) Effect of NF-kappaB and p38 MAPK in activated monocytes/macrophages on pro-inflammatory, cytokines of rats with acute pancreatitis. World J. Gastroenterol., 9, 2513-2518. https://doi.org/10.3748/wjg.v9.i11.2513
  37. Mancuso, C. and Santangelo, R. (2014) Ferulic acid: pharmacological and toxicological aspects. Food Chem. Toxicol., 65, 185-195. https://doi.org/10.1016/j.fct.2013.12.024
  38. Choi, J.H., Park, J.K., Kim, K.M., Lee, H.J. and Kim, S. (2018) In vitro and in vivo antithrombotic and cytotoxicity effects of ferulic acid. J. Biochem. Mol. Toxicol., 32, e22004. https://doi.org/10.1002/jbt.22004
  39. Wang, Y., Deng, Z., Lai, X. and Tu, W. (2005) Differentiation of human bone marrow stromal cells into neural-like cells induced by sodium ferulate in vitro. Cell Mol. Immunol., 2, 225-229.